Download Target or barrier? The cell wall of early- and later

REVIEW ARTICLE
published: 13 March 2015
doi: 10.3389/fpls.2015.00133
Target or barrier? The cell wall of early- and later-diverging
plants vs cadmium toxicity: differences in the response
mechanisms
Luigi Parrotta 1 , Gea Guerriero 2 , Kjell Sergeant 2 , Giampiero Cai 1 * and Jean-Francois Hausman 2 *
1
2
Dipartimento Scienze della Vita, Università di Siena, Siena, Italy
Environmental Research and Innovation, Luxembourg Institute of Science and Technology, Esch-sur-Alzette, Luxembourg
Edited by:
Joanna M.-F. Cross, İnönü
University, Turkey
Reviewed by:
Zoë A. Popper, National University
of Ireland, Ireland
Danuta M. Antosiewicz, University
of Warsaw, Poland
Metin Turan, Yeditepe University,
Turkey
*Correspondence:
Giampiero Cai, Dipartimento
Scienze della Vita, Università di
Siena, via Mattioli 4, I-53100 Siena,
Italy
e-mail: [email protected];
Jean-Francois Hausman,
Environmental Research and
Innovation, Luxembourg Institute of
Science and Technology,
5, Avenue des Hauts-Fourneaux,
L-4362 Esch-sur-Alzette,
Luxembourg
e-mail: jean-francois.hausman@
list.lu
Increasing industrialization and urbanization result in emission of pollutants in the
environment including toxic heavy metals, as cadmium and lead. Among the different
heavy metals contaminating the environment, cadmium raises great concern, as it is
ecotoxic and as such can heavily impact ecosystems. The cell wall is the first structure
of plant cells to come in contact with heavy metals. Its composition, characterized by
proteins, polysaccharides and in some instances lignin and other phenolic compounds,
confers the ability to bind non-covalently and/or covalently heavy metals via functional
groups. A strong body of evidence in the literature has shown the role of the cell wall in
heavy metal response: it sequesters heavy metals, but at the same time its synthesis and
composition can be severely affected. The present review analyzes the dual property of
plant cell walls, i.e., barrier and target of heavy metals, by taking Cd toxicity as example.
Following a summary of the known physiological and biochemical responses of plants to
Cd, the review compares the wall-related mechanisms in early- and later-diverging land
plants, by considering the diversity in cell wall composition. By doing so, common as
well as unique response mechanisms to metal/cadmium toxicity are identified among
plant phyla and discussed. After discussing the role of hyperaccumulators’ cell walls
as a particular case, the review concludes by considering important aspects for plant
engineering.
Keywords: cadmium, plant cell wall, heavy metal stress, heavy metal biosorption, cell wall polysaccharides, lignin
INTRODUCTION
Plants, differently from animals, are sessile organisms and therefore cannot escape from potentially life-threatening conditions.
This, in part, explains the great metabolic plasticity of plant
cells, which have evolved mechanisms enabling them to adapt
to and cope with environmental challenges. Plants growing on
contaminated soils typically display either tolerance or avoidance.
Plants tolerate heavy metals by sequestering them in specific plant
organelles to keep them segregated from vital cellular components, or by the synthesis of enzymes involved in detoxification.
Alternatively, the uptake and translocation of the heavy metal is
decreased. However, there is a wide diversity in the details of the
response, and species- or even clone-specific molecular responses
have been recorded. Cadmium (Cd) is known to be phytotoxic
and to affect plant physiological processes, from roots to shoots.
Adverse effects caused by Cd are of considerable importance for
all plants but, from an agricultural point of view, Cd is a toxic
environmental pollutant that affects crop productivity (Du et al.,
2012). While numerous reports have analyzed the cellular and
enzymatic mechanisms involved in the response to Cd stress in
plants, only a handful of studies have focused on the role of the
plant cell wall. The cell wall is the outermost structure of plant
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cells and therefore the first in contact with the environment. It
has important chemical characteristics, which make it a very good
biosorbent of heavy metals. The presence of different functional
groups (e.g., carboxyl, hydroxyl) deriving from the different wall
polysaccharides favors for instance ion-exchange mechanisms
with wall counter-ions. The cell wall is in its turn affected by heavy
metals, since both its biosynthesis and composition can be altered.
This leads to modifications in its physico-chemical properties
which increase the binding capacity and at the same time lower
the entry of heavy metals in the protoplast (Krzesłowska, 2011).
IMPACT OF Cd POLLUTION ON PLANT CELLS AND ORGANS
Cd can have many consequences on plant physiology. It can affect
both shoot growth and leaf biomass in Zea mays by impairing
chlorophyll synthesis and by promoting the expression of defense
proteins (Lagriffoul et al., 1998). In garlic (Allium sativum), Cd
reduces root growth in a concentration-dependent manner (Liu
et al., 2003).
It is also capable of damaging processes related to plant
reproduction, with logical impacts on plant dispersal and biodiversity. For example, Cd can affect pollen germination and
pollen tube growth by altering the polarization mechanism and
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by inducing abnormalities within the cell, such as blocking cytoplasmic streaming and alteration of the cytoplasmic organization
(Sawidis, 2008). Moreover, in a recent study, the influence of
exposure to a variety of heavy metals on the germination of
23 flax cultivar seeds was assessed. Using root elongation as
the main parameter, large cultivar-dependent differences were
found for some heavy metals (notably Cd, Ni and Co), while
for other metals a more homogenous influence is described
(Soudek et al., 2010).
The impact of Cd on crops can also be exerted by negatively
influencing the translocation of nutrients, especially of minerals;
in Cd-exposed tomato K, Fe, Mn, and Zn are reported to be poorly
translocated in roots, while P and Mn uptake is drastically reduced
in fruits (Moral et al., 1994). In pea, Cd has effects on both roots
and leaves, and a significant inhibition of growth is combined
with a reduction of transpiration and photosynthesis rate, as well
as a general deterioration of the nutrient status (Sandalio et al.,
2001). These are just a few examples describing the broad range
of Cd-caused impacts on plants. For more information on the
overall effects caused by Cd, readers can refer to specific reviews
(Benavides et al., 2005; Qadir et al., 2014).
Cd is essentially absorbed by roots, but it localizes to all plant
organs and tissues. Leaves are usually the preferential accumulation site of Cd. In leaves, Cd accumulates in different regions,
which correspond to less metabolically active areas and to forthcoming necrotic regions. This suggests that an active metabolism
might be required to detoxify Cd in plants and that the absence of
detoxification mechanisms precedes necrotic events (Cosio et al.,
2005). In the leaves of sensitive plants, Cd exerts its toxic activity
by inducing chlorosis, thereby inhibiting growth. The effects
caused by Cd range from morphological changes to reduction
of the photosynthesis rate to decreased transpiration up to cell
apoptosis (Souza et al., 2011).
Cd also affects the structure and function of roots. In Allium
cepa, Cd treatment induces abnormalities, such as extensive vacuolization, condensation of the cytoplasm, damages to mitochondrial cristae, plasmolysis, and condensation of chromatin.
Although dense granules were detected between the cell wall and
the plasma membrane, no specific sites of Cd-accumulation were
found in the cell walls of Allium roots (Liu and Kottke, 2004).
As plants are exposed to different environmental stresses, the
effects of Cd contamination cannot be isolated from injuries
caused by other environmental stresses and it might sometimes
be difficult to predict the combinatory effect (Mittler, 2006). The
simultaneous presence of different stresses might multiply the
negative effects; however, as already observed in rice seedlings, one
type of stress can also partially suppress the effects of another. In
rice, for example, heat stress can ameliorate the negative effects
of Cd pollution through the activation of protective systems
based on anti-oxidant activities (Shah et al., 2013). However,
the study of combined stresses is much less advanced than that
of single stresses, although some studies have been performed
combining Cd-exposure with other treatments (Sergeant et al.,
2014). Given that polluted soils are generally not contaminated
with Cd alone, the exposure of plants to mixtures of metals (Printz
et al., 2013a,b), or the use of real-life polluted soils in experiments
(Evlard et al., 2014a), could give new insights into the metabolic
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The cell wall against cadmium
adjustments of plants when exposed to high concentrations of
trace nutrients.
ROLE OF PHYTOCHELATINS AND METALLOTHIONEINS IN
THE RESPONSE OF PLANTS TO Cd STRESS
Although Cd is a generally toxic contaminant of the ecosystem,
plants have evolved diverse mechanisms to respond to Cd contamination of their growth substrate. As for many compounds
with detrimental effects on cellular metabolism, the toxicity of
Cd is often alleviated through its sequestration to specific cellular
compartments, such as vacuoles, or within specialized cells, such
as trichomes (Harada et al., 2010). Adaptation of plants to Cdcontaminated soils might also rely on the symbiotic cooperation
with other organisms. In Medicago sativa, colonization of roots
by arbuscular mycorrhizae increases the tolerance of plants to Cd
and the decreased Cd toxicity observed is somewhat proportional
to the extent of colonization. It is likely that fungi possess a
battery of enzymatic activities/mechanisms capable of chemically
modifying Cd, thereby making it less toxic (Wang et al., 2012).
The cell wall can act effectively as a biosorbent of Cd, alleviating the toxic effects of this heavy metal. It is clear that the
cell wall-based protection mechanism is only one of the processes
used by plants to cope with the damage induced by Cd. Before
exploring more specifically the molecular mechanisms in which
the cell wall is involved, it is necessary to introduce the other
protective mechanisms with which plants are equipped. These
are based on specialized oligopeptides (namely phytochelatins
and metallothioneins), on biochemical responses and on the
intracellular sequestration of Cd.
Plants can respond by producing specific chelating agents,
such as phytochelatins, that complex with Cd, thereby reducing
its toxic potential (Carrier et al., 2003). The production of phytochelatins coincides with the activation of sulfur metabolism.
This increases the synthesis of cysteine and of reduced glutathione
(GSH), an antioxidant precursor of phytochelatins (Zhang and
Shu, 2006). Increased levels of sulfur can also affect the distribution of Cd in plants by remobilizing it from the cell wall
to the cytosolic compartment. As sulfur is important in the
biosynthesis of sulfhydryl proteins, it is suggested that a higher
content of sulfur generates larger amounts of proteins capable of
sequestering Cd in the cytosol, thereby reducing the accumulation
of the metal in the cell wall (Zhang et al., 2014c). Therefore,
the availability of sulfur might control the synthesis rate of these
sulfur-rich proteins (Loeffler et al., 1989; Uegsegger et al., 1990).
Although this information is inferred from indirect observations
(i.e., by determining that, in the presence of higher levels of sulfur,
Cd is preferentially located in the vacuole), this also suggests that
the balance between cell wall-bound and cytosol-associated Cd
depends on the availability of proteins capable of sequestering Cd.
The use of phytochelatins for the detoxification of Cd-stressed
plants is considered an important mechanism, but its actual role
is still unclear and seems to be organ-dependent. Roots of the
hyperaccumulator Sedum alfredii do not make efficient use of the
phytochelatin-based mechanism for protection against Cd, while
this process is conversely used in the shoots of the same plant
(Zhang et al., 2010b). The use of different tolerance mechanisms
in shoots and roots is also found in other hyperaccumulators
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such as Typha angustifolia, one based on GSH-related antioxidant
systems (in leaves) and the other based on GSH-related chelation
system (in roots; Xu et al., 2011).
An important class of cysteine-rich proteins binding heavy
metals in plants and animals are metallothioneins (MTs). Their
role in heavy metal stress in plants is known and their potential
use in biotechnology is supported by recent studies, which have
analyzed the effects of MTs overexpression in Arabidopsis thaliana
and tobacco (Gu et al., 2014; Zhou et al., 2014). The transformed
plants showed increased tolerance to Cd stress, which was accompanied by a lower accumulation of H2 O2 in A. thaliana and by a
higher ROS scavenging activity in tobacco.
Data in the literature indicate that a universal mechanism
of Cd tolerance is not present and that different, often closelyrelated plants, respond differently when exposed to Cd. For
instance, Cd-tolerant cultivars of black oat (Avena strigosa) accumulate Cd in the leaves, mainly in the cell wall. Those plants
use a phytochelatin-based response when exposed to Cd, but
also induce the up-regulation of ascorbate peroxidase and superoxide dismutase, indicating that an anti-oxidant response is
triggered upon Cd treatment. By contrast, the phytochelatinbased response appears unimportant in Cd- sensitive plants,
although their total content increased upon heavy metal exposure
(Uraguchi et al., 2009).
OTHER FACTORS AFFECTING THE RESPONSE/ADAPTATION/
DEFENSE OF PLANTS TO Cd
The number and diversity of resistance mechanisms used by
plants might be larger than expected. For example, it was reported
that treatment of Cd-stressed plants with salicylic acid alleviates a
number of effects caused by Cd. It is likely that the positive effects
of salicylic acid are not directly correlated with the removal of
Cd, but with the activation of response and defense genes, which
in turn may code for enzymes involved in the maintenance of
homeostasis of plant cells (Moussa and El-Gamal, 2010). Activation of pathogenesis-related defense proteins of the glucanase
family is likely to be a common trait of many plants in response
to Cd. This process was observed in different plants, for instance
maize and soybean treated with Cd and other metals, suggesting
that this defense mechanism is shared by relatively distant species
(Piršelová et al., 2011).
The response of plants to Cd also requires the activation
of enzymes capable of refolding proteins, as one of the most
dramatic effects of intracellular Cd is protein denaturation.
Therefore, some of the enzymes activated during response and
adaptation to Cd belong to the chaperone family and chaperonelike proteins are likely active during the response to Cd pollution.
As Cd can denature proteins, heat-shock proteins (HSPs) are
involved in the refolding of denatured proteins and indeed levels
of HSPs have been reported to increase after Cd treatment (Sergio
et al., 2007). Increased levels of HSP70 were also detected in the
bryophyte Conocephalum conicum exposed to Cd and Pb, suggesting that the need to refold proteins is a prerequisite to maintain
cellular activity during heavy metal stress (Basile et al., 2013).
In pea roots, Cd and Cu treatment were reported to affect
the enzymatic activity of proteins involved in the oxidation and
peroxidation of cell wall components, such as guaiacol peroxi-
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The cell wall against cadmium
dase, ascorbate peroxidase, coniferyl alcohol peroxidase, NADH
oxidase and indole-3-acetic acid (IAA) oxidase (Chaoui et al.,
2004). The evidence that Cd might increase the activity of cell
wall-bound coniferyl alcohol peroxidase is of particular interest
because this enzymatic activity metabolizes coniferyl alcohol, a
monolignol used as substrate presumably involved in the lignification process (Quiroga et al., 2001). This suggests that Cd pollution
might have severe repercussions on the development of secondary
cell walls, by reducing their rigidity and robustness. An increase in
guaiacol peroxidase activity was also reported in lichens exposed
to higher concentrations of Cd (Sanità Di Toppi et al., 2005). As
lichens are fungi-algae symbionts generally resistant and tolerant
to heavy metal pollution, the use of plasma membrane-associated
peroxidases might be a general mechanism to counteract the
negative effects caused by Cd.
Changes in cell wall-associated peroxidase activity were also
observed in roots of Brassica juncea stressed by Cd treatment.
Here, Cd increases the activity of ionically cell wall-bound proteins, thereby increasing peroxidase activity too (Verma et al.,
2008). The upregulated peroxidase activity is supposedly involved
in the adaptation mechanism to Cd stress.
Although specific studies have not been conducted to determine the impact of Cd exposure on the cell wall proteome and
on the diversity of responses in closely related species, numerous
cell wall localized proteins were identified in general proteome
studies on the impact of heavy metal pollution, namely Cd excess,
on plants. These include general stress responsive proteins. For
instance, in a study on two flax cultivars with different tolerance
levels to Cd exposure, the cell wall-localized chitinase increased in
both cultivars, but the protein accumulated at significantly higher
levels in the more tolerant cultivar (Hradilova et al., 2010).
Proteomics studies in poplar found that exposure to Cd
resulted in an increased accumulation of β-1,3-glucanase and
chitinase (Kieffer et al., 2008; Durand et al., 2010). Moreover
Kieffer et al. (2008) identified the significantly higher accumulation of different isoforms of cell wall localized peroxidase, linking
the cell wall and anti-oxidative enzymes found in this compartment with Cd-stress. An intra-specific comparison of different
Populus nigra ecotypes found differences in the mechanism of
tolerance, indicating the variability and highlighting the difficulty
to generate a physiological model, even at the species level. In
Cd-stressed poplar plants, the activity of superoxide dismutase
decreases, while the enzymatic activity of both peroxidase and
catalase increased significantly in roots; this suggests that these
plants trigger a response based on enhanced oxidase activity.
Although the cytology of root cells is significantly altered, these
plants exhibit a considerable capacity as hyperaccumulators and
they have been consequently proposed as phytoremediators (Ge
et al., 2012).
In addition to the various mechanisms outlined above, extracellular compartmentalization is another strategy used by many
plants to limit the injuries caused by Cd. This mechanism involves
the binding and accumulation of Cd in the cell wall, which
serves as a reservoir for Cd. It is capable of concentrating and
accumulating Cd, thus preventing it from penetrating inside the
cell where it can cause damages. In the legume white lupin,
the ability of the cell wall and vacuole-deposited phytochelatins
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to sequester Cd is relatively comparable in stems, but the cell
wall is more effective in both roots and leaves (Vázquez et al.,
2006). This suggests that these organs have specialized cell walls
capable of sequestering Cd, while stems have mostly developed
the phytochelatin-based mechanism for protection against Cd.
Predominant accumulation of Cd in the cell wall of roots was also
observed in Spartina alterniflora (Pan et al., 2012) and Kandelia
obovata (Weng et al., 2012) treated with different concentrations
of Cd. Enhanced accumulation of Cd in the cell wall of leaf cells
was conversely reported in Alternanthera philoxeroides (Xu et al.,
2012a).
Before discussing how Cd affects plant cell wall and how it can
be a barrier against Cd, we need to introduce its key features.
THE PLANT CELL WALL: A LIVING STRUCTURE
Plant cells are enveloped by a layer composed of structural
proteins and polysaccharides (which can be impregnated by the
aromatic polymer lignin), interwoven to form an intricate mesh,
the cell wall. This structure has a complex three-dimensional
organization and is considered an example of a natural biocomposite. The plant cell wall constitutes a material with exceptional
mechanical performance and is taken as a model for the creation
of materials with superior properties.
Cell walls protect the living protoplasts against external insults
but, at the same time, they are very plastic since modifications
in their composition and structure are responsible for enabling
cell growth and development. Two types of cell walls can be
distinguished: primary and secondary cell walls. The first is typically found in actively growing plant cells and is characterized
by the presence of cellulose, pectin and hemicellulose. It is quite
thin and flexible, thus enabling cell expansion (Guerriero et al.,
2014a). Secondary walls are specialized structures synthesized
when plant cells have ceased to elongate. They are responsible for
mechanical strengthening (namely via the deposition of lignin)
and accompany the phase of secondary growth, which determines
the increase in stem girth (Guerriero et al., 2014a,b). The progressive stem thickening ensures resistance to bending. The main
components of secondary walls are cellulose, xylan and lignin
(Cosgrove and Jarvis, 2012).
A third type of wall (more specifically a wall layer) can be
distinguished, which is found in specialized cell types and/or
in response to mechanical stimuli: the gelatinous wall layer (Glayer). This type of wall is characterized by the presence of a
thick layer of crystalline cellulose and is typically found in tension
wood. Cells with a G-layer are also found in the stem of fiber crops
like hemp, flax and nettle and are associated with the phloem.
These cells are very long and known as bast fibers (Mellerowicz
and Gorshkova, 2012; Guerriero et al., 2013).
Besides encasing and shielding plant protoplasts, the cell wall
can be affected by nutritional stress and undergoes variations in
composition. For example grapevine callus subjected to deficiency
in S, N, and P showed walls with a decreased content in cellulose,
increased lignin amount, alterations in the methylesterification
of pectin (Fernandes et al., 2013). These results show how plant
cell walls are remodeled in response to mineral deficits and how
their composition is modified according to the stress condition
applied. The plant cell wall indeed takes active part in transmitting
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The cell wall against cadmium
exogenous signals to the interior of the cells: evidences show the
existence of a cell wall integrity (CWI) maintenance mechanism
which is triggered upon exogenous stresses (Hamann and Denness, 2011; Wolf et al., 2012; Engelsdorf and Hamann, 2014).
The knowledge concerning CWI maintenance is far from being
complete; however, given the similarity existing with that of yeast,
both chemical and physical signals are supposed to contribute to
it (Hamann and Denness, 2011). An example of a physical signal
is represented by the weakening of the cell wall (for instance as
a consequence to treatments with drugs like dichlobenil or isoxaben) up to a point that it can no longer counteract the internal
turgor pressure with consequent cell swelling and bursting. A
weakened wall causes stretching of the plasma membrane and
activation of mechanosensitive channels which trigger an increase
in the cytoplasmic concentration of calcium (Humphrey et al.,
2007; Hamann and Denness, 2011).
Chemical signals are generated upon degradation of the cell
wall by pathogens: for example, pectin-derived oligogalacturonides (OGAs) with a specific length, degree of acetylation
and methylesterification, are capable of inducing rapid defense
responses (Hamann and Denness, 2011; Vallarino and Osorio,
2012; Ferrari et al., 2013). The presence of signals, which allow
the wall to “sense” the status of the cell, implies the existence of
receptors that can intercept those signals. Several receptors have
been described in the literature and among them wall associated
kinases (WAKs) have been well studied. Those receptors are
located in the plasma membrane, but have a domain protruding
into the cell wall and a cytoplasmic kinase domain (Anderson
et al., 2001; Humphrey et al., 2007). Their structure is therefore ideal to create a continuum cell wall-plasma membranecytoplasm and to transfer the signal from the outside to the inside
of the cell. The role of these receptors is particularly interesting
if one considers the relationship existing between heavy metal
stress and water balance within plant cells. Gating of aquaporins
was recorded within 10 min of heavy metal application to onion
epidermal cells, which results in alterations in the turgor pressure
(Przedpelska-Wasowicz and Wierzbicka, 2011). Since the WAKs
membrane receptors are activated upon changes in turgor pressure (a phenomenon observed in pollen grains of Picea wilsonii
after Cd stress; Wang et al., 2014), their functional study could
provide important insights into the sensing mechanism and reveal
downstream players involved in the signaling cascade.
THE CELL WALL AS A BARRIER TO Cd
The composition of the cell wall shows many differences among
phyla and it has played a vital role for their survival throughout
evolution (Sarkar et al., 2009 and references therein). In the
attempt to understand how different taxonomic groups respond
to Cd (or heavy metals in general), it is valuable to compare the
chemical composition and structure of cell walls from different
phyla. Information might shed light either on alternative resistance mechanisms, or on how to improve the strategy used to
tolerate Cd. The rationale at the basis of this assumption is that
the variety of responses to Cd pollution, as found among different
phyla, might be mirrored by molecular and cytological “tricks”
that plants have evolved at the cell wall level. In discussing this
issue, it is necessary to consider that evidence for the cell wall
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acting as a barrier against Cd (and other heavy metals) is not
immediately clear from every study. The availability of molecular
and structural data is low, which leads to fragmented pictures
strongly affecting the development of a unifying model. Moreover, it is not possible to rule out that a unifying model does not
exist and therefore it is necessary to present individual situations.
The ability of either a plant cell or a plant in toto to tolerate Cd can
be implemented at different levels and with different mechanisms.
In the attempt to outline the different resistance mechanisms in
which cell walls are involved, it is possible to rank them based on
(a) the morphology of the barrier organ (for example the root),
(b) the transport capacity of the contaminant, (c) the absorption
of Cd into the cell wall by polysaccharides or proteins, (d) the
impediment of Cd to penetrate through the plasma membrane.
The first part of the section aims at surveying the wall-related
strategies developed by early- and later-diverging embryophytes.
Charophytes, the closest algal relatives of embryophytes, are also
briefly treated, given their importance in the study of land plant
cell wall origin (Sørensen et al., 2011; Mikkelsen et al., 2014).
The second part of the section discusses the mechanisms of Cd
absorption/translocation in different plant organs and tissues,
while considering the cell wall organization/composition.
PLANT CELL WALL ACROSS DIFFERENT PHYLA: COMPOSITION AND
MECHANISMS OF RESISTANCE TO Cd
Charophyte cell walls possess high amounts of mannosecontaining hemicellulose, glucuronic acid, mannuronic acid, 3O-methyl rhamnose (Popper and Fry, 2003) and possess neither
lignin nor cutin. More importantly, they are capable of calcifying
and calcite is known to bind and sequester heavy metals (Gomes
and Asaeda, 2013). The macrophyte alga Chara australis can
accumulate Cd and be used for remediation of contaminated soils
(Clabeaux et al., 2013). Studies carried out on another species of
macrophyte, Chara fragilis, showed that binding of uranyl species
to the cell walls was mainly due to the presence of calcite (Daković
et al., 2008). The biomineralization potential of Charophytes is
therefore very promising for phycoremediation (i.e., the use of
algae for the removal of pollutants) and further studies should be
performed to link the cell wall composition of these algae to their
calcifying potential.
Bryophytes, a group of early-diverging non-vascular plants,
possess walls with mannose-containing hemicellulose, uronic
acids and 3-O-methyl rhamnose, similarly to Charophytes (Sarkar
et al., 2009). They lack lignin, although they contain lignans
and other lignin-like polymers (Sarkar et al., 2009 and references
therein). Bryophytes are known bioindicators of heavy metal
pollution and their walls show high biosorption capacity because
of the numerous ion-exchange sites (e.g., from uronic acids).
The wall of the moss Pohlia drummondii was shown to form,
together with the plasma membrane, an efficient shield against
elevated zinc doses (Lang and Wernitznig, 2011); therefore, the
living protoplast is protected from harmful effects. The moss Scorpiurum circinatum treated with different heavy metals, including
Cd, immobilized the toxic ions in the cell walls, which is therefore
used as the main detoxification site (Basile et al., 2012).
The Pteridophytes, another group of early-diverging plants,
are very interesting organisms, as their cell walls show special-
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The cell wall against cadmium
ization to support the differentiation of a vascular tissue: galactomannan, glucomannan are abundant in secondary walls of
leptosporangiates and lignin, together with xylan, has also been
observed (Sarkar et al., 2009 and references therein). In the fern
Lygodium japonicum it was shown that the wall pectins bind
copper via homogalacturonans (Konno et al., 2005). In Salvinia
auriculata Cd was shown to induce severe deformations at the
cell wall level. Moreover an opaque layer could be observed along
the middle lamella (Wolff et al., 2012). This finding might be
explained by the binding capacity of pectins, the chief component
of middle lamellas, a feature which is shared by seed plants.
Among Pteridophytes, Equisetales certainly deserve attention, as
their walls show the occurrence of mixed-linkage glucans and
they are known for their biosilicification activity. Interestingly, a
relationship was proposed between these hemicelluloses and Si
mineralization (Fry et al., 2008). It would be interesting to investigate whether the sequestration of heavy metals by Equisetales
takes place via mixed-linkage glucans.
These data indicate that the cell wall is a target for the accumulation of Cd in early-diverging plants, such as Bryophytes and
Pteridophytes. These organisms use molecular mechanisms that
are compatible with the chemical composition of their cell wall.
However, as outlined above, both the structure and composition
of the cell wall changed during evolution and it is therefore
expected that chemically-different cell walls might respond differently to Cd pollution. The in-depth study of early-diverging plant
cell wall biosynthesis and composition can reveal fine molecular
details and inspire further avenues for improving the cell wall
capacity to accumulate toxic heavy metals (see section “Future
outlook”).
In later-diverging plants (such as spermatophytes), the increasing number of tissues and organs, coupled with the more sophisticated architecture, also generated cell walls with an increasing
variability at the chemical and physical level. Consequently, it is
likely that the diversity in Cd tolerance extends to the organ, tissue
and even to the cellular level (see next paragraph).
In seed plants, and more specifically in flowering plants, most
of the information was obtained from a limited number of species
and, sometimes, on crop plants.
The evidence that the cell wall can exert a protective role was
supported by studying Cd toxicity in crop plants. Pea plants were
shown to be more sensitive than maize plants to Cd exposure;
compared to pea plants, maize plants exhibited a higher percentage of cell wall-associated Cd, while pea showed higher content of
Cd in the cytoplasm (Lozano-Rodríguez et al., 1997). This finding
suggests that the cell wall acts as a barrier, preventing Cd from
entering the cytoplasm where it is extremely toxic for plant cells.
It is consequential that different cell wall structures and textures
might bind Cd differently and thus provide different levels of
protection. Comparable results were found in strawberry, where
the treatment with different concentrations of Cd highlighted
that the cell wall of leaves and roots is the primary reservoir for
Cd, with root cell walls showing higher binding capacity than
leaf cell walls (Zhang et al., 2010a). The fact that roots display a
higher accumulating capacity than leaves can be an index of their
protective activity preventing the entry and accumulation of Cd
in the cytoplasm. If the concept of the cell wall as a barrier is true,
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the differential accumulating capacity of plant cell walls has to
be found in their chemical and physical diversity. This diversity
can cover not only the polysaccharide component of the cell wall,
but also the protein fraction or modifications induced on one, the
other or both components.
PLANT CELL WALL COMPOSITION IN DIFFERENT ORGANS AND
TISSUES: LINK WITH Cd ABSORPTION AND TRANSLOCATION
Since Cd is primarily adsorbed at the root level, it follows that
the anatomy and molecular structure of the cell wall in root cells
is a critical parameter. Findings in different plant species indicate
that roots with higher content of suberin and lignin may be more
impermeable to Cd and therefore more resistant to its absorption
and translocation (Lux, 2010). Increased accumulation of suberin
was observed in the roots of the monocotyledonous medicinal
plant Merwilla plumbea exposed to Cd, a process interpreted
as a protective response against penetration of Cd in the cells
(Lux et al., 2011). The presence of root mucilage is another
factor playing an important role in Cd adsorption, as shown in
sunflower (Yang and Pan, 2013). The differential structure of roots
might explain why Cd translocation is different between plants
and variable even within the same taxonomic group.
Screening of different clones of Salix grown on identical reallife soil revealed remarkable differences in the translocation of
Cd and other metals (Evlard et al., 2014b). Similar differences
were found in solanaceous plants (Yamaguchi et al., 2011), different poplar species (He et al., 2013) and between ecotypes of
the hyperaccumulators Thlaspi caerulescens and T. praecox (Xing
et al., 2008).
In plants restraining Cd in roots, Cd is sequestered in the
endoderm and the cortical regions of roots. When this filter
fails, Cd can penetrate the xylem vessels and translocate to the
shoot. Therefore, the specific composition of cell walls in the
endoderm and cortex is critical (Akhter et al., 2014). Ultimately,
the cell wall of roots is considered as an effective barrier against
penetration of Cd and a relationship can be established between
higher accumulation of Cd in the roots vs lower accumulation in
the leaves (Sun et al., 2013). This suggests that Cd-tolerance goes
through the capacity of roots to limit the diffusion of Cd towards
the entire plant.
The protective activity exerted by the cell wall may not only
depend on the polysaccharide fraction, but also on other cell
wall molecules that can bind Cd and other heavy metals. As
earlier suggested by Sanità Di Toppi and Gabbrielli (1999), the
response of later-diverging plants to Cd may involve different
types of molecular mechanisms, from the phytochelatin-based
sequestration, to cell wall immobilization and plasma membrane
exclusion, to the use of stress proteins. In this context, the cell wall
(by acting as a molecular barrier) may be part of both adaptation
mechanisms to permanent pollution and response mechanisms
to acute stress. However, additional factors might be required to
achieve full functionality and protection against Cd pollution.
In fact, in addition to the binding of Cd to polysaccharides and
proteins, tolerance to Cd might also involve the sequestration of
Cd complexes in the cell wall. In crop plants such as maize and
wheat, addition of P concomitantly to Cd treatment increased
the tolerance of plants to Cd (Zhimin et al., 1999). P may
Frontiers in Plant Science | Plant Genetics and Genomics
The cell wall against cadmium
associate with Cd thereby generating insoluble complexes that
remain within the cell wall. Combination of binding to P and
polysaccharides is also possible.
Therefore, the addition of P to contaminated soils seems to
modify their physiochemical status, making Cd less available for
plants, thereby improving the tolerance of plants to Cd pollution.
In addition, Cd accumulates more consistently in the cell wall of
plants growing on P-supplemented soils, which therefore hinder
its entry in the cytoplasm (Siebers et al., 2013).
If the differential capacity of plants to resist Cd is linked to the
chemical variability of their cell walls, it is clear that such variability can be consistently increased by modifying the protein component of the cell wall. Specific cell wall proteins could provide
an additional barrier by binding Cd and thus preventing it from
penetrating into the cytoplasm. In barley treated with Ni and/or
Cd, the apoplastic fraction of leaves showed increased amount
of apoplastic proteins that accumulate concomitantly with the
metal treatment (Blinda et al., 1997). Therefore, the response
of plants to contaminating metals may also involve the specific
de novo synthesis of proteins that potentially make plants more
tolerant. Proteins not directly involved in Cd binding have also
been reported to increase Cd tolerance in plants. As previously
discussed, an example is represented by cysteine-rich proteins
as identified in Digitaria ciliaris and Oryza sativa. The genes
coding for these proteins were found to be upregulated following
Cd treatment and transgenic plants overexpressing cysteine-rich
proteins are more tolerant to Cd stress by preventing entry into
the cytoplasm (Kuramata et al., 2009). This finding also highlights
the possibility of manipulating plants in order to increase their
mechanisms of tolerance to pollutant agents.
Accumulation of Cd in the cell wall (or more generally in
the apoplast) is also dependent on the efficient transport of Cd
through the plasma membrane so that cytoplasmic Cd can be
transported outside and incorporated in the cell wall. While doing
so, the content of cytoplasmic Cd decreases while Cd accumulates
in the cell wall. Transport of Cd through the plasma membrane is
likely dependent on membrane transporters. Their involvement
is also suggested by indirect evidence showing that, while Cd
is promptly adsorbed in the cell wall, its influx in the symplast
is linear with Cd concentration, which suggests the activity of
low-affinity transport systems (Redjala et al., 2009). Recently
the transporter IRT1 (IRON-REGULATED TRANSPORTER 1)
was shown to be not only involved in the uptake of iron,
but also of toxic metals, among which Cd (Barberon et al.,
2014). This root transporter is recycled via a mechanism involving a phosphatidylinositol-3-phosphate-binding protein, FYVE1,
which controls its delivery to the outer plasma membrane domain
of root epidermal cells.
These observations stress the importance of studying the cell
wall structure of both tolerant and resistant plants in order
to identify those molecules that provide the highest protection
against Cd. One example of an important molecule is lignin. The
protective activity of lignin is suggested by pretreatment of wheat
plants with wheat germ agglutinin, which generally exerts an amelioration of Cd effects. This pretreatment likely involves a different
balance between hormone levels but an important phenotypic
effect is an accelerated lignification of cell walls (Bezrukova et al.,
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Parrotta et al.
FIGURE 1 | How the cell wall can act as a barrier against Cd pollution.
Plant cells can counteract the toxicity of Cd in several ways and the cell
wall actively participates to most of these mechanisms. Apart from
mechanisms of sequestration based on the activity of vacuoles and
phytochelatins, additional decontaminating activities can be exerted by the
cell wall. For example, specific polysaccharides of the cell wall can bind Cd
2011). Such secondary modifications might render cell walls less
permeable to Cd thus limiting its entry in the cell. Lignin can
also bind Cd thereby inhibiting its diffusion into the cells. Higher
abundance of lignin in secondary cell walls might thus make
plants more tolerant to the effects of Cd treatment.
In Pisum sativum leaves, lignin was shown to be deposited
following Cd stress and this process was accompanied by an
oxidative burst in the xylem vessel cell walls (Rodríguez-Serrano
www.frontiersin.org
The cell wall against cadmium
through sulfated moieties (although this situation is restricted to very few
cases, e.g., seaweeds and vascular plants adapted to inhabit saline
environments). Cd might also be sequestered in the cell wall by the activity
of either cell wall-associated proteins or cell wall phosphates. An additional
barrier might be represented by secondary modifications of the cell wall,
such as lignin deposition.
et al., 2009). Moreover, Cd was shown to favor the process of
xylogenesis, by inducing the activity of enzymes via H2 O2 accumulation (Schützendübel et al., 2001). The use of sophisticated
labeling techniques involving quantum dot technologies can highlight the interaction between Cd and specific cell wall components
(Djikanovic et al., 2012). The multitude of activities of the cell wall
as a barrier against Cd pollution is schematically summarized in
Figure 1.
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Parrotta et al.
THE CELL WALL AS TARGET: EFFECTS OF Cd ON CELL WALL
SYNTHESIS AND COMPOSITION
In the previous paragraphs, the cell wall has been considered as
a potential reservoir for Cd and thus as an efficient barrier to
its penetration in the plant. In some cases, Cd is not efficiently
neutralized and it might become an injuring factor by affecting
the structure of cell walls. The toxic activity of Cd can be exerted
at different levels. Cd can alter the physical structure of the
cell wall by interacting with negatively charged molecules (i.e.,
carboxyl groups and sulfates). In this way, Cd can substantially
modify the cell wall resistance to turgor pressure thereby making
the cells weaker. In addition to interacting with the polysaccharide component, Cd can interfere with the enzymatic activities
present in the cell walls by inhibiting the enzymatic reactions
that strengthen the cell wall structure. Furthermore, Cd can
affect directly or indirectly the synthesis of cell wall components, or interfere with the transport of the latter to the final
destination.
Presence of Cd also affects the deposition pattern of pectins.
In the hypocotyl of Linum usitatissimum, the presence of an
excess of Cd changes the ratio between low and high methylesterified pectins, causing the former to accumulate consistently
in epidermal cells and determining the collapse of the subepidermal cell layer (Douchiche et al., 2007). This unbalance
affects the primary walls and may cause swelling of hypocotyl
tissues. It is not clear how Cd determines such effects, but it is
likely that it alters the expression level of pectin-metabolizing
enzymes such as pectin methyl-esterase (PME). Overexpression
of this enzyme can change the ratio between low and high
methyl-esterified pectins by altering their level of esterification.
This leads to a relatively higher abundance of acidic pectins
and extremely impairs the shaping of plant cells, which is based
on a precise balance in degree of esterification. In addition to
changing the degree of esterification of pectins, Cd can also
affect more generally the chemistry of these polysaccharides for
example by altering the expression of peroxidases, which in their
turn alter the chemical structure of homogalacturonans (Paynel
et al., 2009). The effects caused by Cd on the development
of cell walls and, more specifically, on pectins might be more
subtle and not immediately appreciable. This is the case for
flax fibers where Cd treatment affects the deposition of secondary cell walls in terms of adhesion of cellulose microfibrils.
On the contrary, the effects on both low and high methylesterified pectins are not immediately explicable (Douchiche
et al., 2011).
That pectins are important in binding Cd is demonstrated by
experiments with plants grown in P deficiency. Lower levels of
P alleviate the negative effects caused by Cd because P reduces
the content of pectins and PME in the cell wall. The reduced
level of this enzyme enhances the ratio between low and high
methyl-esterified pectins further, making a lower number of active
sites available for Cd binding, thereby triggering a heavy metalexclusion mechanism (Zhu et al., 2012).
Further studies on the role of pectins in response to Cd
exposure were carried out in rice. The addition of NO donors
concurrently with Cd treatment makes plants more resistant to
Cd injuries. The resistance is mainly based on the overproduction
Frontiers in Plant Science | Plant Genetics and Genomics
The cell wall against cadmium
of pectins and on the simultaneous reduction of cellulose levels
(Xiong et al., 2009). It is likely that pectins are Cd adsorbent via
carboxylic groups, thus preventing the metal from entering the
cytoplasm. It would be fascinating to analyze if NO donors alter
the expression of genes coding for enzymes involved in pectin
synthesis. The possible role of NO in alleviating the symptoms
caused by Cd treatment has been already reviewed (Xiong et al.,
2010).
The evidence that toxic elements such as heavy metals could
bind to pectin in the cell walls has been already observed and
described (Malovikova and Kohn, 1982). There is a vast literature
on the chemical interaction between heavy metals and pectins
(Krzesłowska, 2011) although the exact mechanism of damage
caused by Cd on pectins is not completely clear. It is likely that
Cd can substitute calcium ions thereby modifying the rigidity
of the pectin skeleton. This fact has been suggested in the alga
Ulva lactuca where the rhamnose subunits are cross-linked by
calcium and the replacement of calcium by Cd can decrease
the rigidity of the cell wall (Webster and Gadd, 1996). It is
noteworthy that calcium can alleviate the injuries caused by Cd,
likely either because calcium can compete for the binding to
cell wall polysaccharides, or Cd might use calcium channels to
penetrate inside cells (Suzuki, 2005). At the cellular level, Cd can
induce remarkable aberrations on the cell wall structure resulting
in changes in cell shape (Sawidis and Reiss, 1995; Sawidis, 2008).
These observations are consistent with the hypothesis that Cd
interferes with the process of cell wall structuring probably by
altering the exact arrangement of pectins. In some experimental
cases, exposure to soils contaminated with Cd induces a general increase of the levels of pectin and a reduction of methylesterified pectins (Astier et al., 2014). Nevertheless, understanding
exactly the alterations induced by Cd on the structure of the
pectin skeleton is not simple and the use of antibodies directed
against different chemical forms of pectin cannot help to define
exactly how Cd damages the pectin cell wall (Douchiche et al.,
2011).
Direct effects of Cd on the synthesis of other polysaccharides
(such as cellulose and callose) are not known. However, it was
reported that Cd triggers the accumulation of specific Cd-induced
glycine-rich proteins (cdiGRPs). These are cell wall-associated
proteins that might positively regulate the synthesis of callose.
The cdiGRPs likely work in cooperation with an additional cell
wall protein, the so-called GrIP (cdiGRP-interacting protein;
Ueki and Citovsky, 2005). The model proposed by the authors
suggests that Cd increases the post-translational accumulation of
cdiGRP, which is also dependent on the expression of GrIP. Once
accumulated in the cell wall, cdiGRP enhances the production
and/or accumulation of callose, which consequently represents
a cell wall adaptation to Cd pollution. Accumulation of callose
in response to metal stress probably does not involve altered
mechanisms of callose removal. In maize and soybean, treatment
with metals (including Cd) induces the accumulation of callose in
the cell wall. Results indicate that the accumulation is not related
to decreased enzymatic activity of glucanases and reinforce the
hypothesis that accumulation of callose is primarily dependent
on a higher rate of synthesis and/or deposition (Piršelová et al.,
2012). Like callose, there are few reports on the relationship
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Parrotta et al.
between Cd and cellulose and the relationship between Cd
pollution and cellulose synthesis is far from being completely
understood.
The effects of Cd on cell wall synthesis might also be indirect.
Cd is known to affect the level of apoplastic sucrose probably by altering the activity of cell wall invertase. Consequently,
sucrose accumulates in the cell wall and decreases in the cytoplasm (Podazza et al., 2006). Lower levels of cytoplasmic sucrose
can have detrimental effects on cell wall synthesis by making
substrates for the biosynthesis of cell wall precursors less available. Synthesis of both cellulose and callose requires the addition of UDP-glucose, which can be produced by two different
metabolic pathways. The first requires the enzyme UDP-glucose
pyrophosphorylase (UGPase) that catalyzes the reversible production of UDP-glucose and pyrophosphate from glucose-1phosphate and UTP; the second mechanism involves the activity of sucrose synthase, which breaks down sucrose (in the
presence of UTP) into UDP-glucose and fructose (Kleczkowski
et al., 2010). Lower levels of cytoplasmic sucrose may reduce
the activity of sucrose synthase and consequently may lower
the production rate of UDP-glucose. As sucrose synthase is
associated with both callose synthase and cellulose synthase
(Brill et al., 2011), it follows that the Cd-induced reduction of
cytoplasmic sucrose might affect the synthesis of cellulose and
callose.
Another pathway by which Cd can affect the synthesis and
deposition of cell wall is indirect and relates to the effects of
Cd on cytoplasmic streaming. It is known that delivery of cell
wall synthesizing enzymes requires an intact cytoskeleton and an
intact membrane system: cell wall synthesizing enzymes traffic
along the cytoskeleton, which guides the enzymes towards the
final insertion sites in the plasma membrane (Crowell et al.,
2010). The precise balance between insertion and removal of cell
wall synthesizing enzymes is critical to correctly deposit the cell
wall and to assemble a proper cell wall texture. Cd affects the
intracytoplasmic movement of organelles and vesicles in the epidermal cells of the model plant A. cepa (Wierzbicka et al., 2007).
Cytoplasmic streaming disorders are likely to impact negatively on
the cell wall assembly. We do not know how Cd affects organelle
streaming, if through an unspecific pathway (for example, by
altering the ionic homeostasis of cells), or a more specific mechanism that directly inhibits the proteins involved in organelle
transport. Nevertheless, it is clear that Cd has a considerable
influence on the structure of actin filaments and consequently
on cytoplasmic streaming. In A. thaliana root hairs, Cd alters the
balance between influx and efflux of Ca2+ , which consequently
abolishes the Ca2+ gradient. Since Ca2+ regulates the dynamics
of actin filaments in tip-growing cells, the Cd-induced imbalance
of Ca2+ has negative effects on actin filaments that consecutively
impair the motility of organelles and vesicles, as reviewed by
Wan and Zhang (2012). As observed by the authors, the cell
wall structure is also affected because of the altered cytoplasmic
streaming (Fan et al., 2011). The relationship between Cd and
Ca2+ is likely more complex than expected in view of the finding
that a member of the plant cadmium-resistance (PCR) protein
family is a Ca2+ efflux transporter, which is involved in the finer
regulation of intracellular Ca2+ concentration (Song et al., 2011).
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The cell wall against cadmium
The global effects of Cd on cell wall synthesis are summarized in
Figure 2.
Cd ACCUMULATION IN PLANTS: THE CASE OF
HYPERACCUMULATORS AND THE EFFECT OF NUTRIENTS
In the previous sections, data concerning how Cd can be a
harmful element for plants and how plants can respond to damage
caused by Cd were presented and discussed. Emphasis was put
on how evolutionarily-distant plants can respond in different
ways to Cd treatment; this is an indication that several different
mechanisms have evolved in response to Cd. In this section, the
focus will be put on those plants showing heavy metal hyperaccumulating capacity, since they represent an extreme case. Moreover,
the study of their cell walls can lead to important observations,
which can be transferred to biotechnological approaches. In this
section considerations on the role of macro- and micro-nutrients
in the increased Cd accumulation/tolerance will also be made,
since this aspect is linked with the potential of enhancing the plant
capacity to accumulate Cd.
Hyperaccumulator plants are characterized by the extraordinary capacity of accumulating Cd and of translocating it towards
the aerial parts of plants (namely leaves) and of detoxifying
the element locally (Rascio and Navari-Izzo, 2011). At the level
of leaves, Cd can be accumulated in specific sites, such as the
vacuoles or the cell wall. It is therefore possible to assume that
in hyperaccumulators the ability of the cell wall to absorb Cd is
so high that Cd fails to actively penetrate inside the cytoplasm
and remains confined within the cell wall. Even if the molecular
mechanisms working in hyperaccumulator plants are the same
as those present in Cd-resistant plants, the main difference is
that the former can concentrate Cd in the cell wall at extreme
levels without apparent damage. There are many examples of
hyperaccumulators and, as the study is continuing, new species
are added to this list. The root hairs of T. caerulescens, a metal
hyperaccumulator, can accumulate consistent levels of Cd in
their cell walls thereby preventing Cd from penetrating in the
cytoplasm (Nedelkoska and Doran, 2000). Massive accumulation
of Cd in hyperaccumulator plants is also based on complexes with
phosphates within the cell wall. However, not all cell types accumulate Cd at the same level (Küpper et al., 2000). Accumulation
of Cd and Zn may have particular relevance in hyperaccumulator
plants, such as Sedum plumbizincicola, in which heavy metals are
chiefly accumulated in shoots and relatively less in roots (Cao
et al., 2014). Dittrichia viscosa is another model-accumulator
plant that accumulates large amounts of Cd in the cell wall
(Fernández et al., 2014).
The ability of certain species to accumulate Cd is linked
not only to the higher ROS scavenging activity, but also to Fe
homeostasis: studies carried out on the Cd-accumulator Solanum
nigrum and the low Cd-accumulating Solanum torvum showed
that Cd treatment caused a lower Fe accumulation in S. torvum
compared to S. nigrum (Xu et al., 2012b). This difference is related
to the increased expression of Fe transporters, namely IRT1, and
IRT2, in the roots of the Cd-accumulator S. nigrum (Xu et al.,
2012b).
The most important application of hyperaccumulator plants
is linked to the possibility of decontaminating polluted sites
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FIGURE 2 | Effects of Cd on cell wall synthesis. Cd might affect the
synthesis of cell wall components in many different ways. First, Cd can
affect the activity of pectin methyl-esterase (PME) that consequently affects
the balance between methyl-esterified and unesterified pectins. In turn, this
alters the elasticity of the cell wall. Second, Cd might affect the structure of
cellulose directly or indirectly by affecting the delivery of cellulose synthase
(see also “Future outlook”). Consequently, researchers are looking
for hyperaccumulators that can be used to detoxify contaminated
soils in an economically feasible and reasonable way. This has
been already proposed for two species of Iris (Han et al., 2007).
Those plants, capable of restoring optimal conditions in contaminated soils, have evolved molecular mechanisms to tolerate
high concentrations of contaminants. The acquisition of tolerance
to contaminants involves the development of mechanisms for
Frontiers in Plant Science | Plant Genetics and Genomics
The cell wall against cadmium
(CesA). The indirect interfering activity can be exerted by damaging the actin
filament structure or by affecting the uptake of sucrose (which provides the
metabolites for cell wall synthesis). Cd is also hypothesized to affect the
synthesis of callose by interfering with regulatory proteins. Finally, Cd can
also modify the lignification level of the cell wall, by acting on related
enzymes.
the accumulation of pollutants in specific cell sites, such as the
vacuole and cell wall of root cells where Cd might be complexed
with insoluble phosphates that strongly limit the translocation of
Cd to aboveground tissues and organs (Zhang et al., 2014b). This
suggests that the hyperaccumulating capacity of cell walls can be
induced or improved by adding specific chemical groups. This can
involve both the polysaccharide and the protein component of
the cell wall. In this respect, studies on transgenic tobacco plants
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Parrotta et al.
overexpressing a xyloglucan endotransglucosylase/hydrolase gene
support this statement. In those plants, xyloglucans accumulated
at lower levels, which prevents plants from binding Cd. This
suggests that xyloglucans could be relevant binding sites for Cd
and are involved in Cd tolerance; conversely, plants with lower
levels of xyloglucans accumulate lower amounts of this heavy
metal (Han et al., 2014).
Another significant example is represented by the addition of
Si. Si considerably reduced the net influx of Cd by likely producing
Si-cell wall complexes that efficiently adsorb Cd thus preventing
its entry in the cytoplasm (Liu et al., 2013). In such a way,
the cell wall can be potentiated, thus becoming a more effective
barrier against Cd. The ameliorating activity of Si is dependent
on its concentration, as well as on the concentration of Cd, and
Si has a major effect on Cd influx by modifying the cell wall
texture. However, Si does not affect intracellular processes like
photosynthesis (Lukacová et al., 2013). In mangrove plants, Si is
known to alleviate the effects of Cd pollution by restricting Cd
to the cell wall of roots and reducing the concentration of Cd in
the symplast. Therefore Si enhances the capacity of cell walls to
restrain Cd, thereby limiting its diffusion (Zhang et al., 2014a).
The possibility of improving the hyperaccumulator capacity of
plants may not be simple, as the number of genes involved may
be huge. A preliminary assay in the hyperaccumulator S. alfredii
revealed that plants under Cd stress respond by modifying the
expression level of more than 100 genes responsible for different
functions (including cell wall modification; Gao et al., 2013).
Comparable analyses by using suppression subtractive hybridization screens showed that the activity of several genes is important
in making plants of Salix caprea tolerant to Cd pollution. Some of
the investigated genes belong to the family of cell wall modifying
enzymes (Konlechner et al., 2013). This finding opens the way to
the identification of potential genes (and gene products) capable
of raising the tolerance capacity of plants against Cd.
The study of hyperaccumulators’ cell walls will lead to the
identification of those functional chemical groups capable of
absorbing high amounts of Cd thereby preventing its entry in
the cytoplasm. In addition to understanding the chemistry of this
process, it is also necessary to identify the cellular mechanisms
allowing the addition of such chemical groups in the cell wall (e.g.,
specific enzymes that modify the chemical structure of cell wall
components). It follows that the development of hyperaccumulator plants requires a high level of knowledge. Ideally, the most
convenient result would be to combine the hyperaccumulating
capacity of non-crop plants (in which this process has been widely
studied) with the economically advantageous crop plants. By
transferring the genetic information at the base of Cd resistance
into crop plants, it will be possible to design improved plants
capable at the same time to detoxify the soil and to maintain the
soil productivity rate (Wu et al., 2010).
PLANT BIOTECHNOLOGY AND Cd TOXICITY: WHAT SHOULD
BE CONSIDERED?
The examples listed previously show that plants are equipped with
different mechanisms to cope with the toxicity induced by heavy
metals (Cd, specifically). Studying the variety of responses will
allow us to identify specific mechanisms used to tolerate large
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The cell wall against cadmium
doses of pollutant. Those mechanisms (based either on chelating
proteins, on general biochemical responses, or on sequestering in
the vacuole/cell wall) may not necessarily be present in plants of
economic interest and may concern either plant products or plant
waste. For example, an interesting applicative aspect concerning
the detoxifying ability of cell walls is the use of waste vegetable
components rich in pectins as biosorbent of heavy metals (Wan
Ngah and Hanafiah, 2008). The knowledge of these biosorbent
mechanisms can be used to develop plants capable of sequestering
Cd (hyperaccumulators; Douchiche et al., 2010). Pectins can also
find applications outside the plant context. Fruits rich in pectin
can absorb significant amounts of heavy metals (Schiewer and
Patil, 2008). Such technologies can be extended to pectin gels
extracted from commercial plants, such as sugar beet. Such studies, in addition to demonstrating that pectin-enriched matrices
can actually be applied for Cd removal, confirm that Cd binds
pectin matrices by removing calcium ions (Mata et al., 2009,
2010). Other food wastes have been proposed in this regard, for
example citrus peels (Schiewer and Iqbal, 2010).
Several studies have shown altered Cd accumulation in plants
engineered to express genes involved in heavy metal uptake,
translocation or chelation. For example, as previously mentioned,
tobacco plants expressing the Zn and Cd translocator HMA4 from
A. thaliana, which controls translocation to the shoot (Wong
and Cobbett, 2009), show decreased Cd accumulation, but also
deep transcriptional remodeling leading to increased lignification
(Siemianowski et al., 2014). Restricting the examples to the cell
wall, which is the topic of this review, the upregulation of a peroxidase, O-methyltransferase and hydroxycinnamoyl reductase leads
to an increased deposition of lignin in a specific layer between
the root epidermis and the first cortical layer, which consequently
blocks Cd apoplastic movement towards the stele (Siemianowski
et al., 2014). These transgenic tobacco plants exposed to Cd,
however, show an enhanced Fe and Zn deficiency status linked
to the overexpression of two metal uptake genes, ZIP1 and IRT1
(Siemianowski et al., 2014). These results show how challenging
biotechnological prospects for improving heavy metal tolerance
in plants are, as plants overexpressing a specific gene might show
unfavorable/unexpected features linked to the response of the
host to the transgene.
The insertion of new genes whose products change the chemical structure of cell wall might be a way to engineer plants that are
more Cd-resistant. An alternative strategy would be to introduce
specific mutations in genes already present. Mutation in one gene
coding for a specific cellulose synthase subunit significantly alters
the content of cellulose and decreases the cell wall thickness in rice
plants. Although there were no clear phenotypical differences in
comparison to control plants, mutant plants showed a significant
decrease in the translocation rate of Cd along xylem vessels,
which appeared as abnormal in shape. The new morphological
structure of xylem, although not impairing the total shape of
plants, determines a consistent reduction in the transport of
Cd to leaves, thereby making rice plants more tolerant to Cd
pollution (Song et al., 2013). Together with other studies, this
finding highlighted that the translocation of Cd from roots to
shoots is likely more critical than the mere uptake of Cd at the
root level (Xin et al., 2013). Therefore, the accumulation of Cd
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Parrotta et al.
in the leaves seems more closely related to the translocation rate
than to Cd uptake and reinforces the necessity of studying how
Cd is translocated through the xylem and the factors that can be
modified/regulated to delay such process.
The presence of the so-called “metal cross-homeostasis” has
been identified as a primary factor influencing the phenotype
of plants with a modified expression of genes involved in metal
homeostasis (Antosiewicz et al., 2014). This cross-homeostasis is
primarily due to the cross-talk existing between the homeostatic
mechanisms of different metals: for example the concentration of
different metals regulates the same players of the transcriptional
wiring, the same transporters and chelators (Antosiewicz et al.,
2014).
Approaches in biotechnology represent the most effective
way to engineer heavy metal accumulation in plants. In particular, three elements are relevant to devise effective engineering approaches for heavy metal uptake/accumulation in plants:
(1) the choice of specific promoters, for instance tissue-specific
promoters (Antosiewicz et al., 2014), which restrict eventual
modifications to a specific tissue or organ; (2) integrative studies
aimed at deciphering the response of plants to a specific metal at
a transcriptional, protein and metabolic level; (3) the choice of
the host to express a specific transgene. This last feature is very
relevant, as fast-growing plants with high biomass yield should be
preferred. As an example, fiber crops like hemp (Cannabis sativa
L.) represent very good candidates for engineering approaches.
Hemp has a deep root system, a fast growth rate and is known to
require less water than other crops (like cotton): all these features
make it extremely interesting for biotechnology. Moreover the
hemp genome has been sequenced (van Bakel et al., 2011), a
feature which can greatly favor the design of constructs, e.g.,
for synthetic biology. Last but not least, the tissues of hemp
stems show a great diversity of chemical composition: the core
is lignified, while the cortex is rich in cellulosic bast fibers.
This heterogeneity in cell wall composition offers a variety of
functional groups potentially useful for heavy metal sequestration
in hemp stem tissues.
FUTURE OUTLOOK: WHAT COMES NEXT?
To conclude this review, a list of points that need further study is
hereafter proposed to achieve a more comprehensive knowledge
of the mechanisms involved in Cd toxicity in plants and to devise
new strategies for the biotechnological improvement of plant
tolerance to toxic heavy metals.
(1) Studying how early- and later-diverging plants progressively
adapted and responded to Cd will reveal a particular mechanism or even a combination of molecular mechanisms, which
could be used to improve the response of crop plants grown
on contaminated soils. In this context the coupling of–omics
sciences (transcriptomics, proteomics, metabolomics) and
advanced imaging techniques (namely mass spectrometry
imaging, like Secondary Ion Mass Spectrometry, SIMS) can
generate a wealth of information covering different levels of
biological complexity.
(2) Considering the chemical variety of cell walls and the potential diversity in polysaccharide and protein composition,
Frontiers in Plant Science | Plant Genetics and Genomics
The cell wall against cadmium
there might be several possibilities for the cell wall to interfere
with the toxic activity of Cd. Therefore, the study of cell walls
(in terms of assembly and composition) in hyperaccumulators can provide important information on how to improve
the survival or the productivity of plants growing on Cdcontaminated soils. In this context, it is important to identify
the natural targets of Cd at the cell wall level and to figure
out which of these targets can be modified to prevent the
negative effects of Cd. One approach to develop this point
is the functional study of those targets via generation of
mutants/overexpressors. The purpose of this approach is to
generate plants that either cannot absorb Cd or can sequester
Cd in the cell wall thereby reducing or avoiding detrimental
effects in terms of growth or productivity.
(3) Studies on the effects induced at the cell wall-level by the
application of beneficial mineral nutrients deserve further
attention. In particular the role of Si and P in alleviating
the toxic effects of Cd should be analyzed via an integrative
biology approach to identify the targets of this interaction.
ACKNOWLEDGMENTS
GG, KS, and JFH thank partial financial support obtained
through the National Research Fund, FNR Project CANCAN
C13/SR/57742025774202 and project CADWALL INTER/FWO/
12/14. The authors also thank Lucien Hoffmann for critical reading. The conceiving of this Review is linked to activities conducted
within the COST FP1105 and COST FP1106 actions.
REFERENCES
Akhter, M. F., Omelon, C. R., Gordon, R. A., Moser, D., and Macfie, S. M. (2014).
Localization and chemical speciation of cadmium in the roots of barley and
lettuce. Environ. Exp. Bot. 100, 10–19. doi: 10.1016/j.envexpbot.2013.12.005
Anderson, C. M., Wagner, T. A., Perret, M., He, Z. H., He, D., and Kohorn, B. D.
(2001). WAKs: cell wall-associated kinases linking the cytoplasm to the extracellular matrix. Plant Mol. Biol. 47, 197–206. doi: 10.1023/A:1010691701578
Antosiewicz, D. M., Barabasz, A., and Siemianowski, O. (2014). Phenotypic and
molecular consequences of overexpression of metal-homeostasis genes. Front.
Plant Sci. 5:80. doi: 10.3389/fpls.2014.00080
Astier, C., Gloaguen, V., and Faugeron, C. (2014). Phytoremediation of
cadmium-contaminated soils by young douglas fir trees: effects of cadmium exposure on cell wall composition. Int. J. Phytorem. 16, 790–803. doi:
10.1080/15226514.2013.856849
Barberon, M., Dubeaux, G., Kolb, C., Isono, E., Zelazny, E., and Vert, G. (2014).
Polarization of IRON-REGULATED TRANSPORTER 1 (IRT1) to the plant-soil
interface plays crucial role in metal homeostasis. Proc. Natl. Acad. Sci. U.S.A.
111, 8293–8298. doi: 10.1073/pnas.1402262111
Basile, A., Sorbo, S., Conte, B., Cardi, M., and Esposito, S. (2013). Ultrastructural
changes and Heat Shock Proteins 70 induced by atmospheric pollution are
similar to the effects observed under in vitro heavy metals stress in Conocephalum conicum (Marchantiales–Bryophyta). Environ. Pollut. 182, 209–216.
doi: 10.1016/j.envpol.2013.07.014
Basile, A., Sorbo, S., Pisani, T., Paoli, L., Munzi, S., and Loppi, S. (2012).
Bioacumulation and ultrastructural effects of Cd, Cu, Pb, and Zn in the moss
Scorpiurum circinatum (Brid.) Fleisch. Loeske. Environ. Pollut. 166, 208–211.
doi: 10.1016/j.envpol.2012.03.018
Benavides, M. P., Gallego, S. M., and Tomaro, M. L. (2005). Cadmium toxicity in
plants. Braz. J. Plant Physiol. 17, 21–34. doi: 10.1590/S1677-04202005000100003
Bezrukova, M. V., Fatkhutdinova, R. A., Lubyanova, A. R., Murzabaev, A. R.,
Fedyaev, V. V., and Shakirova, F. M. (2011). Lectin involvement in the development of wheat tolerance to cadmium toxicity. Russ. J. Plant Physiol. 58, 1048–
1054. doi: 10.1134/S1021443711060021
Blinda, A., Koch, B., Ramanjulu, S., and Dietz, K. J. (1997). De novo synthesis and accumulation of apoplastic proteins in leaves of heavy metal-
March 2015 | Volume 6 | Article 133 | 12
Parrotta et al.
exposed barley seedlings. Plant Cell Environ. 20, 969–981. doi: 10.1111/j.13653040.1997.tb00674.x
Brill, E., van Thournout, M., White, R. G., Llewellyn, D., Campbell, P. M., Engelen,
S., et al. (2011). A novel isoform of sucrose synthase is targeted to the cell wall
during secondary cell wall synthesis in cotton fiber. Plant Physiol. 157, 40–54.
doi: 10.1104/pp.111.178574
Cao, D., Zhang, H., Wang, Y., and Zheng, L. (2014). Accumulation and distribution characteristics of zinc and cadmium in the hyperaccumulator plant
Sedum plumbizincicola. Bull. Environ. Contam. Toxicol. 93, 171–176. doi:
10.1007/s00128-014-1284-8
Carrier, P., Baryla, A., and Havaux, M. (2003). Cadmium distribution and microlocalization in oilseed rape (Brassica napus) after long-term growth on cadmiumcontaminated soil. Planta 216, 939–950. doi: 10.1007/s00425-002-0947-6
Chaoui, A., Jarrar, B., and El Ferjani, E. (2004). Effects of cadmium and copper on
peroxidase, NADH oxidase and IAA oxidase activities in cell wall, soluble and
microsomal membrane fractions of pea roots. J. Plant Physiol. 161, 1225–1234.
doi: 10.1016/j.jplph.2004.02.002
Clabeaux, B. L., Navarro, D. A., Aga, D. S., and Bisson, M. A. (2013). Combined
effects of cadmium and zinc on growth, tolerance, and metal accumulation in
Chara australis and enhanced phytoextraction using EDTA. Ecotoxicol. Environ.
Saf. 98, 236–243. doi: 10.1016/j.ecoenv.2013.08.014
Cosgrove, D. J., and Jarvis, M. C. (2012). Comparative structure and biomechanics of plant primary and secondary cell walls. Front. Plant Sci. 3:204. doi:
10.3389/fpls.2012.00204
Cosio, C., De Santis, L., Frey, B., Diallo, S., and Keller, C. (2005). Distribution
of cadmium in leaves of Thlaspi caerulescens. J. Exp. Bot. 56, 765–775. doi:
10.1093/jxb/eri062
Crowell, E. F., Gonneau, M., Stierhof, Y. D., Höfte, H., and Vernhettes, S. (2010).
Regulated trafficking of cellulose synthases. Curr. Opin. Plant Biol. 13, 700–705.
doi: 10.1016/j.pbi.2010.07.005
Daković, M., Kovacević, M., Andjus, P. R., and Bacić, G. (2008). On the mechanism
of uranium binding to cell wall of Chara fragilis. Eur. Biophys. J. 37, 1111–1117.
doi: 10.1007/s00249-008-0282-3
Djikanovic, D., Kalauzi, A., Jeremic, M., Xu, J., Micic, M., Whyte, J. D., et al. (2012).
Interaction of the CdSe quantum dots with plant cell walls. Colloids Surf. B
Biointerfaces 91, 41–47. doi: 10.1016/j.colsurfb.2011.10.032
Douchiche, O., Driouich, A., and Morvan, C. (2011). Impact of cadmium on early
stages of flax fibre differentiation: ultrastructural aspects and pectic features of
cell walls. Plant Physiol. Biochem. 49, 592–599. doi: 10.1016/j.plaphy.2011.03.
008
Douchiche, O., Rihouey, C., Schaumann, A., Driouich, A., and Morvan, C. (2007).
Cadmium-induced alterations of the structural features of pectins in flax
hypocotyl. Planta 225, 1301–1312. doi: 10.1007/s00425-006-0425-7
Douchiche, O., Soret-Morvan, O., Chaïbi, W., Morvan, C., and Paynel, F. (2010).
Characteristics of cadmium tolerance in ‘Hermes’ flax seedlings: contribution of
cell walls. Chemosphere 81, 1430–1436. doi: 10.1016/j.chemosphere.2010.09.011
Du, Y. P., Li, H. J., Yin, K. L., and Zhai, H. (2012). Cadmium accumulation,
subcellular distribution, and chemical forms in Vitis vinifera cv. Chardonnay
grapevine. Chi. J. Appl. Ecol. 23, 1607–1612.
Durand, T. C., Sergeant, K., Planchon, S., Carpin, S., Label, P., Morabito, D., et al.
(2010). Acute metal stress in Populus tremula × P. alba (717-1B4 genotype): leaf
and cambial proteome changes induced by cadmium2+ . Proteomics 10, 349–368.
doi: 10.1002/pmic.200900484
Engelsdorf, T., and Hamann, T. (2014). An update on receptor-like kinase involvement in the maintenance of plant cell wall integrity. Ann. Bot. 114, 1339–1347.
doi: 10.1093/aob/mcu043
Evlard, A., Sergeant, K., Printz, B., Guignard, C., Renaut, J., Campanella, B.,
et al. (2014a). A multiple-level study of metal tolerance in Salix fragilis and
Salix aurita clones. J. Proteom. 101, 113–129. doi: 10.1016/j.jprot.2014.02.
007
Evlard, A., Sergeant, K., Ferrandis, S., Printz, B., Renaut, J., Guignard, C., et al.
(2014b). Physiological and proteomic responses of different willow clones (Salix
fragilis × alba) exposed to dredged sediment contaminated by heavy metals. Int.
J. Phytorem. 16, 1148–1169. doi: 10.1080/15226514.2013.821448
Fan, J. L., Wei, X. Z., Wan, L. C., Zhang, L. Y., Zhao, X. Q., Liu, W. Z., et al.
(2011). Disarrangement of actin filaments and Ca2+ gradient by CdCl2 alters
cell wall construction in Arabidopsis thaliana root hairs by inhibiting vesicular trafficking. J. Plant Physiol. 168, 1157–1167. doi: 10.1016/j.jplph.2011.01.
031
www.frontiersin.org
The cell wall against cadmium
Fernandes, J. C., García-Angulo, P., Goulao, L. F., Acebes, J. L., and Amâncio,
S. (2013). Mineral stress affects the cell wall composition of grapevine (Vitis
vinifera L.) callus. Plant Sci. 205–206, 111–120. doi: 10.1016/j.plantsci.2013.
01.013
Fernández, R., Fernández-Fuego, D., Bertrand, A., and González, A. (2014). Strategies for Cd accumulation in Dittrichia viscosa (L.) Greuter: role of the cell wall,
non-protein thiols and organic acids. Plant Physiol. Biochem. 78, 63–70. doi:
10.1016/j.plaphy.2014.02.021
Ferrari, S., Savatin, D. V., Sicilia, F., Gramegna, G., Cervone, F., and Lorenzo,
G. D. (2013). Oligogalacturonides: plant damage-associated molecular patterns and regulators of growth and development. Front. Plant Sci. 4:49. doi:
10.3389/fpls.2013.00049
Fry, S. C., Nesselrode, B. H. W. A., Miller, J. G., and Mewburn, B. R. (2008).
Mixed linkage (1–3,1–4)- β-D-glucan is a major hemicellulose of Equisetum
(horsetail) cell walls. New Phytol. 179, 104–115. doi: 10.1111/j.1469-8137.2008.
02435.x
Gao, J., Sun, L., Yang, X., and Liu, J. X. (2013). Transcriptomic analysis of cadmium
stress response in the heavy metal hyperaccumulator Sedum alfredii Hance. PLoS
ONE 8:e64643. doi: 10.1371/journal.pone.0064643
Ge, W., Jiao, Y. Q., Sun, B. L., Qin, R., Jiang, W. S., and Liu, D. H. (2012). Cadmiummediated oxidative stress and ultrastructural changes in root cells of poplar
cultivars. S. Afr. J. Bot. 83, 98–108. doi: 10.1016/j.sajb.2012.07.026
Gomes, P. I., and Asaeda, T. (2013). Phytoremediation of heavy metals by calcifying macro-algae (Nitella pseudoflabellata): implications of redox insensitive
end products. Chemosphere 92, 1328–1334. doi: 10.1016/j.chemosphere.2013.
05.043
Gu, C. S., Liu, L. Q., Zhao, Y. H., Deng, Y. M., Zhu, X. D., and Huang, S. Z. (2014).
Overexpression of Iris lactea var. chinensis metallothionein llMT2a enhances
cadmium tolerance in Arabidopsis thaliana. Ectoxicol. Environ. Safe. 105, 22–28.
doi: 10.1016/j.ecoenv.2014.04.002
Guerriero, G., Sergeant, K., and Hausman, J. F. (2013). Integrated -omics: a
powerful approach to understanding the heterogeneous lignification of fibre
crops. Int. J. Mol. Sci. 14, 10958–10978. doi: 10.3390/ijms140610958
Guerriero, G., Hausman, J. F., and Cai, G. (2014a). No stress! Relax! Mechanisms
governing growth and shape in plant cells. Int. J. Mol. Sci. 15, 5094–5114. doi:
10.3390/ijms15035094
Guerriero, G., Sergeant, K., and Hausman, J. F. (2014b). Wood biosynthesis and
typologies: a molecular rhapsody. Tree Physiol. 34, 839–355. doi: 10.1093/treephys/tpu031
Hamann, T., and Denness, L. (2011). Cell wall integrity maintenance in plants:
lessons to be learned from yeast? Plant Sign. Behav. 6, 1706–1709. doi:
10.4161/psb.6.11.17782
Han, Y. L., Yuan, H. Y., Huang, S. Z., Guo, Z., Xia, B., and Gu, J. (2007). Cadmium
tolerance and accumulation by two species of Iris. Ecotoxicology 16, 557–563.
doi: 10.1007/s10646-007-0162-0
Han, Y., Sa, G., Sun, J., Shen, Z., Zhao, R., Ding, M., et al. (2014). Overexpression of Populus euphratica xyloglucan endotransglucosylase/hydrolase
gene confers enhanced cadmium tolerance by the restriction of root cadmium uptake in transgenic tobacco. Environ. Exp. Bot. 100, 74–83. doi:
10.1016/j.envexpbot.2013.12.021
Harada, E., Kim, J. A., Meyer, A. J., Hell, R., Clemens, S., and Choi, Y. E. (2010).
Expression profiling of tobacco leaf trichomes identifies genes for biotic and
abiotic stresses. Plant Cell Physiol. 51, 1627–1637. doi: 10.1093/pcp/pcq118
He, J. L., Ma, C. F., Ma, Y. L., Li, H., Kang, J. Q., Liu, T. X., et al. (2013).
Cadmium tolerance in six poplar species. Environ. Sci. Poll. Res. 20, 163–174.
doi: 10.1007/s11356-012-1008-8
Hradilova, J., Rehulka, P., Rehulkova, H., Vrbova, M., Griga, M., and Brzobohaty,
B. (2010). Comparative analysis of proteomic changes in contrasting flax cultivars upon cadmium exposure. Electrophoresis 31, 421–431. doi: 10.1002/elps.
200900477
Humphrey, T. V., Bonetta, D. T., and Goring, D. R. (2007). Sentinels at the wall:
cell wall receptors and sensors. New Phytol. 176, 7–21. doi: 10.1111/j.14698137.2007.02192.x
Kieffer, P., Dommes, J., Hoffmann, L., Hausman, J. F., and Renaut, J. (2008).
Quantitative changes in protein expression of cadmium-exposed poplar plants.
Proteomics 8, 2514–2530. doi: 10.1002/pmic.200701110
Kleczkowski, L. A., Kunz, S., and Wilczynska, M. (2010). Mechanisms of
UDP-glucose synthesis in plants. Crit. Rev. Plant Sci. 29, 191–203. doi:
10.1080/07352689.2010.483578
March 2015 | Volume 6 | Article 133 | 13
Parrotta et al.
Konlechner, C., Türktas, M., Langer, I., Vaculík, M., Wenzel, W. W., Puschenreiter,
M., et al. (2013). Expression of zinc and cadmium responsive genes in leaves of
willow (Salix caprea L.) genotypes with different accumulation characteristics.
Environ. Pollut. 178, 121–127. doi: 10.1016/j.envpol.2013.02.033
Konno, H., Nakato, T., Nakashima, S., and Katoh, K. (2005). Lygodium japonicum
fern accumulates copper in the cell wall pectin. J. Exp. Bot. 56, 1923–1931. doi:
10.1093/jxb/eri187
Krzesłowska, M. (2011). The cell wall in plant cell response to trace metals:
polysaccharide remodeling and its role in defense strategy. Acta Physiol. Plant.
33, 35–51. doi: 10.1007/s11738-010-0581-z
Küpper, H., Lombi, E., Zhao, F. J., and McGrath, S. P. (2000). Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 212, 75–84. doi: 10.1007/s004250000366
Kuramata, M., Masuya, S., Takahashi, Y., Kitagawa, E., Inoue, C., Ishikawa, S., et
al. (2009). Novel cysteine-rich peptides from Digitaria ciliaris and Oryza sativa
enhance tolerance to cadmium by limiting its cellular accumulation. Plant Cell
Physiol. 50, 106–117. doi: 10.1093/pcp/pcn175
Lagriffoul, A., Mocquot, B., Mench, M., and Vangronsveld, J. (1998). Cadmium
toxicity effects on growth, mineral and chlorophyll contents, and activities of
stress related enzymes in young maize plants (Zea mays L.). Plant Soil 200, 241–
250. doi: 10.1023/A:1004346905592
Lang, I., and Wernitznig, S. (2011). Sequestration at the cell wall and plasma
membrane facilitates zinc tolerance in the moss Pohlia drummondii. Environ.
Exp. Bot. 74, 186–193. doi: 10.1016/j.envexpbot.2011.05.018
Liu, D., Jiang, W., and Gao, X. (2003). Effects of cadmium on root growth, cell
division and nucleoli in root tip cells of garlic. Biol. Plantar. 47, 79–83. doi:
10.1023/A:1027384932338
Liu, D., and Kottke, I. (2004). Subcellular localization of cadmium in the root cells
of Allium cepa by electron energy loss spectroscopy and cytochemistry. J. Biosci.
29, 329–335. doi: 10.1007/BF02702615
Liu, J., Ma, J., He, C., Li, X., Zhang, W., Xu, F., et al. (2013). Inhibition of cadmium
ion uptake in rice (Oryza sativa) cells by a wall-bound form of silicon. New
Phytol. 200, 691–699. doi: 10.1111/nph.12494
Loeffler, S., Hochberger, A., Grilli, E., Gekeler, W., Winnacker, E. L., and Zenk,
M. H. (1989). Termination of the phytochelatin synthase reactions through
sequestration of heavy metals by reaction products. FEBS Lett. 258, 42–46. doi:
10.1016/0014-5793(89)81611-4
Lozano-Rodríguez, E., Hernández, L. E., Bonay, P., and Carpena-Ruiz, R. O.
(1997). Distribution of cadmium in shoot and root tissues of maize and pea
plants: physiological disturbances. J. Exp. Bot. 48, 123–128. doi: 10.1093/jxb/48.
1.123
Lukacová, Z., Švubová, R., Kohanová, J., and Lux, A. (2013). Silicon mitigates the
Cd toxicity in maize in relation to cadmium translocation, cell distribution,
antioxidant enzymes stimulation and enhanced endodermal apoplasmic barrier development. Plant Growth Regul. 70, 89–103. doi: 10.1007/s10725-0129781-4
Lux, A. (2010). Does diversity in root structure affect the diversity in cadmium
uptake by plants? Opinion paper. Agrochimica 54, 342–352.
Lux, A., Vaculik, M., Martinka, M., Liskova, D., Kulkarni, M. G., Stirk, W. A., et al.
(2011). Cadmium induces hypodermal periderm formation in the roots of the
monocotyledonous medicinal plant Merwilla plumbea. Ann. Bot. 107, 285–292.
doi: 10.1093/aob/mcq240
Malovikova, A. and Kohn, R. (1982). Binding of cadmium cations to pectins. Collec.
Czech. Chem. Commun. 47, 702–708.
Mata, Y. N., Blázquez, M. L., Ballester, A., González, F., and Muñoz, J. A. (2009).
Sugar-beet pulp pectin gels as biosorbent for heavy metals: preparation and
determination of biosorption and desorption characteristics. Chem. Eng. J. 150,
289–301. doi: 10.1016/j.cej.2009.01.001
Mata, Y. N., Blázquez, M. L., Ballester, A., González, F., and Munoz, J. A.
(2010). Studies on sorption, desorption, regeneration and reuse of sugarbeet pectin gels for heavy metal removal. J. Haz. Mat. 178, 243–248. doi:
10.1016/j.jhazmat.2010.01.069
Mellerowicz, E. J., and Gorshkova, T. A. (2012). Tensional stress generation in
gelatinous fibres: a review and possible mechanism based on cell-wall structure
and composition. J. Exp. Bot. 63, 551–565. doi: 10.1093/jxb/err339
Mikkelsen, M. D., Harholt, J., Ulvskov, P., Johansen, I. E., Fangel, J. U., Doblin,
M. S., et al. (2014). Evidence for land plant cell wall biosynthetic mechanisms in charophyte green algae. Ann. Bot. 114, 1217–1236. doi: 10.1093/aob/
mcu171
Frontiers in Plant Science | Plant Genetics and Genomics
The cell wall against cadmium
Mittler, R. (2006). Abiotic stress, the field environment and stress combination.
Trends Plant Sci. 11, 15–19. doi: 10.1016/j.tplants.2005.11.002
Moral, R., Gomez, I., Pedreno, J. N., and Mataix, J. (1994). Effects of cadmium on
nutrient distribution, yield, and growth of tomato grown in soilless culture. J.
Plant Nutr. 17, 953–962. doi: 10.1080/01904169409364780
Moussa, H. R., and El-Gamal, S. M. (2010). Role of salicylic acid in regulation of
cadmium toxicity in wheat (Triticum aestivum L.). J. Plant Nutr. 33, 1460–1471.
doi: 10.1080/01904167.2010.489984
Nedelkoska, T. V., and Doran, P. M. (2000). Hyperaccumulation of cadmium
by hairy roots of Thlaspi caerulescens. Biotech. Bioeng. 67, 607–615. doi:
10.1002/(SICI)1097-0290(20000305)67:5<607::AID-BIT11>3.0.CO;2-3
Pan, X., Liu, F. C., Chai, M. W., Liu, L. M., Morita, S., and Shi, F. C. (2012). Accumulation, translocation, and subcellular distribution of cadmium in Spartina
alterniflora. Chi. J. Ecol. 31, 526–531.
Paynel, F., Schaumann, A., Arkoun, M., Douchiche, O., and Morvan, C. (2009).
Temporal regulation of cell-wall pectin methylesterase and peroxidase isoforms in cadmium-treated flax hypocotyl. Ann. Bot. 104, 1363–1372. doi:
10.1093/aob/mcp254
Piršelová, B., Kuna, R., Libantová, J., Moravciková, J., and Matušíkova, I. (2011).
Biochemical and physiological comparison of heavy metal-triggered defense
responses in the monocot maize and dicot soybean roots. Mol. Biol. Rep. 38,
3437–3446. doi: 10.1007/s11033-010-0453-z
Piršelová, B., Mistríková, V., Libantová, J., Moravcíková, J., and Matušíková, I.
(2012). Study on metal-triggered callose deposition in roots of maize and
soybean. Biologia 67, 698–705. doi: 10.2478/s11756-012-0051-8
Podazza, C., Rosa, M., González, J. A., Hilal, M., and Prado, F. E. (2006). Cadmium
induces changes in sucrose partitioning, invertase activities, and membrane
functionality in roots of rangpur lime (Citrus limonia L. Osbeck). Plant Biol.
8, 706–714. doi: 10.1055/s-2006-924171
Popper, Z. A., and Fry, S. C. (2003). Primary cell wall composition of bryophytes
and charophytes. Ann. Bot. 91, 1–12. doi: 10.1093/aob/mcg013
Printz, B., Sergeant, K., Lutts, S., Guignard, C., Renaut, J., and Hausman, J. F.
(2013a). From tolerance to acute metabolic deregulation: contribution of proteomics to dig into the molecular response of alder species under a polymetallic
exposure. J. Proteome Res. 12, 5160–5179. doi: 10.1021/pr400590d
Printz, B., Sergeant, K., Guignard, C., Renaut, J., and Hausman, J. F. (2013b).
Physiological and proteome study of sunflowers exposed to a polymetallic
constraint. Proteomics 13, 1993–2015. doi: 10.1002/pmic.201200400
Przedpelska-Wasowicz, E. M., and Wierzbicka, M. (2011). Gating of aquaporins by
heavy metals in Allium cepa L. epidermal cells. Protoplasma 248, 663–671. doi:
10.1007/s00709-010-0222-9
Qadir, S., Jamshieed, S., Rasool, S., Ashraf, M., Akram, N. A., and Ahmad, P.
(2014). “Modulation of plant growth and metabolism in cadmium-enriched
environments,” in Reviews of Environmental Contamination and Toxicology,
ed. D. M. Whitacre (Cham: Springer International Publishing), 51–88. doi:
10.1007/978-3-319-03777-6_4
Quiroga, M., de Forchetti, S. M., Taleisnik, E., and Tigier, H. A. (2001). Tomato
root peroxidase isoenzymes: kinetic studies of the coniferyl alcohol peroxidase
activity, immunological properties and role in response to salt stress. J. Plant
Physiol. 158, 1007–1013. doi: 10.1078/0176-1617-00304
Rascio, N., and Navari-Izzo, F. (2011). Heavy metal hyperaccumulating plants: how
and why do they do it? And what makes them so interesting? Plant Sci. 180,
169–181. doi: 10.1016/j.plantsci.2010.08.016
Redjala, T., Sterckeman, T., and Morel, J. L. (2009). Cadmium uptake by roots:
contribution of apoplast and of high- and low-affinity membrane transport systems. Environ. Exp. Bot. 67, 235–242. doi: 10.1016/j.envexpbot.2009.
05.012
Rodríguez-Serrano, M., Romero-Puertas, M. C., Pazmiño, D. M., Testillano,
P. S., Risueño, M. C., del Río, L. A., et al. (2009). Cellular response of
pea plants to cadmium toxicity: crosstalk between reactive oxygen species,
nitric oxide and calcium. Plant Physiol. 150, 229–243. doi: 10.1104/pp.108.
131524
Sandalio, L. M., Dalurzo, H. C., Gomez, M., Romero-Puertas, M. C., and Del
Rio, L. A. (2001). Cadmium-induced changes in the growth and oxidative
metabolism of pea plants. J. Exp. Bot. 52, 2115–2126. doi: 10.1093/jexbot/52.364.
2115
Sanità Di Toppi, L., and Gabbrielli, R. (1999). Response to cadmium in
higher plants. Environ. Exp. Bot. 41, 105–130. doi: 10.1016/S0098-8472(98)
00058-6
March 2015 | Volume 6 | Article 133 | 14
Parrotta et al.
Sanità Di Toppi, L., Marabottini, R., Vattuone, Z., Musetti, R., Favali, M. A.,
Sorgonà, A., et al. (2005). Cell wall immobilisation and antioxidant status of
Xanthoria parietina thalli exposed to cadmium. Funct. Plant Biol. 32, 611–618.
doi: 10.1071/FP04237
Sarkar, P., Bosneaga, E., and Auer, M. (2009). Plant cell walls throughout evolution:
towards a molecular understanding of their design principles. J. Exp. Bot. 60,
3615–3635. doi: 10.1093/jxb/erp245
Sawidis, T. (2008). Effect of cadmium on pollen germination and tube growth
in Lilium longiflorum and Nicotiana tabacum. Protoplasma 233, 95–106. doi:
10.1007/s00709-008-0306-y
Sawidis, T., and Reiss, H. D. (1995). Effects of heavy metals on pollen tube growth
and ultrastructure. Protoplasma 185, 113–122. doi: 10.1007/BF01272851
Schiewer, S., and Patil, S. B. (2008). Pectin-rich fruit wastes as biosorbents for heavy
metal removal: equilibrium and kinetics. Bioresour. Technol. 99, 1896–1903. doi:
10.1016/j.biortech.2007.03.060
Schiewer, S., and Iqbal, M. (2010). The role of pectin in Cd binding by orange
peel biosorbents: a comparison of peels, depectinated peels and pectic acid. J.
Hazard. Mater. 177, 899–907. doi: 10.1016/j.jhazmat.2010.01.001
Schützendübel, A., Schwarz, P., Teichmann, T., Gross, K., Langenfeld-Heyser, R.,
Godbold, D. L., et al. (2001). Cadmium-induced changes in antioxidative
systems, hydrogen peroxide content, and differentiation in scots pine roots.
Plant Physiol. 127, 887–898. doi: 10.1104/pp.010318
Sergeant, K., Kieffer, P., Dommes, J., Hausmann, J. F., and Renaut, J. (2014).
Proteomic changes in leaves of poplar exposed to both cadmium and lowtemperature. Environ. Exp. Bot. 106, 112–123. doi: 10.1016/j.envexpbot.2014.
01.007
Sergio, E., Cobianchi, R. C., Sorbo, S., Conte, B., and Basile, A. (2007). Ultrastructural alterations and HSP 70 induction in Elodea canadensis Michx. exposed to
heavy metals. Caryologia 60, 115–120. doi: 10.1080/00087114.2007.10589557
Shah, K., Singh, P., and Nahakpam, S. (2013). Effect of cadmium uptake and heat
stress on root ultrastructure, membrane damage and antioxidative response in
rice seedlings. J. Plant Biochem. Biotech. 22, 103–112. doi: 10.1007/s13562-0120116-3
Siebers, N., Siangliw, M., and Tongcumpou, C. (2013). Cadmium uptake and
subcellular distribution in rice plants as affected by phosphorus: soil and hydroponic experiments. J. Soil Sci. Plant Nutr. 13, 833–844. doi: 10.4067/S071895162013005000066
Siemianowski, O., Barabasz, A., Kendziorek, M., Ruszczynska, A., Bulska, E.,
Williams, L. E., et al. (2014). HMA4 expression in tobacco reduces Cd accumulation due to the induction of the apoplastic barrier. J. Exp. Bot. 65, 1125–1139.
doi: 10.1093/jxb/ert471
Song, W. Y., Choi, K. S., De Alexis, A., Martinoia, E., and Lee, Y. (2011). Brassica
juncea plant cadmium resistance 1 protein (BjPCR1) facilitates the radial
transport of calcium in the root. Proc. Natl. Acad. Sci. U.S.A. 108, 19808–19813.
doi: 10.1073/pnas.1104905108
Song, X. Q., Liu, L. F., Jiang, Y. J., Zhang, B. C., Gao, Y. P., Liu, X. L., et al. (2013).
Disruption of secondary wall cellulose biosynthesis alters cadmium translocation and tolerance in rice plants. Mol. Plant 6, 768–780. doi: 10.1093/mp/sst025
Sørensen, I., Pettolino, F. A., Bacic, A., Ralph, J., Lu, F., O’Neill, M. A., et al. (2011).
The charophycean green algae provide insights into the early origins of plant cell
walls. Plant J. 68, 201–211. doi: 10.1111/j.1365-313X.2011.04686.x
Soudek, P., Katrusáková. A., Sedlácek, L., Petrová, S., Kocí, V., Marsík, P., et al.
(2010). Effect of heavy metals on inhibition of root elongation in 23 cultivars
of flax (Linum usitatissimum L.). Arch. Environ. Contam. Toxicol. 59, 194–203.
doi: 10.1007/s00244-010-9480-y
Souza, V. L., De Almeida, A. A. F., Lima, S. G. C., De, M. C., Da, C. S., Mangabeira, P.
A. O., et al. (2011). Morphophysiological responses and programmed cell death
induced by cadmium in Genipa americana L. (Rubiaceae). Biometals 24, 59–71.
doi: 10.1007/s10534-010-9374-5
Sun, J., Cui, J., Luo, C., Gao, L., Chen, Y., and Shen, Z. (2013). Contribution of cell
walls, nonprotein thiols, and organic acids to cadmium resistance in two cabbage varieties. Arch. Environ. Contam. Toxicol. 64, 243–252. doi: 10.1007/s00244012-9824-x
Suzuki, N. (2005). Alleviation by calcium of cadmium-induced root growth inhibition in Arabidopsis seedlings. Plant Biotech. 22, 19–25. doi: 10.5511/plantbiotechnology.22.19
Uegsegger, A., Schmuts, D., and Brunold, C. (1990). Regulation of glutathione
synthesis by cadmium in Pisum sativum L. Plant Physiol. 93, 1579–1584. doi:
10.1104/pp.93.4.1579
www.frontiersin.org
The cell wall against cadmium
Ueki, S., and Citovsky, V. (2005). Identification of an interactor of cadmium
ion-induced glycine-rich protein involved in regulation of callose levels in
plant vasculature. Proc. Natl. Acad. Sci. U.S.A. 102, 12089–12094. doi: 10.1073/
pnas.0505927102
Uraguchi, S., Kiyono, M., Sakamoto, T., Watanabe, I., and Kuno, K. (2009).
Contributions of apoplasmic cadmium accumulation, antioxidative enzymes
and induction of phytochelatins in cadmium tolerance of the cadmiumaccumulating cultivar of black oat (Avena strigosa Schreb.). Planta 230, 267–276.
doi: 10.1007/s00425-009-0939-x
Vallarino, J. G., and Osorio, S. (2012). Signaling role of oligogalacturonides
derived during cell wall degradation. Plant Sign. Behav. 7, 1447–1449. doi:
10.4161/psb.21779
van Bakel, H., Stout, J. M., Cote, A. G., Tallon, C. M., Sharpe, A. G., Hughes, T. R.,
et al. (2011). The draft genome and transcriptome of Cannabis sativa. Genome
Biol. 12, R102. doi: 10.1186/gb-2011-12-10-r102
Vázquez, S., Goldsbrough, P., and Carpena, R. O. (2006). Assessing the relative contributions of phytochelatins and the cell wall to cadmium resistance
in white lupin. Physiol. Plant. 128, 487–495. doi: 10.1111/j.1399-3054.2006.
00764.x
Verma, K., Shekhawat, G. S., Sharma, A., Mehta, S. K., and Sharma, V. (2008).
Cadmium induced oxidative stress and changes in soluble and ionically bound
cell wall peroxidase activities in roots of seedling and 3-4 leaf stage plants of
Brassica juncea (L.) czern. Plant Cell Rep. 27, 1261–1269. doi: 10.1007/s00299008-0552-7
Wan, L., and Zhang, H. (2012). Cadmium toxicity effects on cytoskeleton, vesicular
trafficking and cell wall construction. Plant Sign. Behav. 7, 345–348. doi:
10.4161/psb.18992
Wan Ngah, W. S., and Hanafiah, M. A. K. M. (2008). Removal of heavy metal
ions from wastewater by chemically modified plant wastes as adsorbents:
a review. Bioresour. Technol. 99, 3935–3948. doi: 10.1016/j.biortech.2007.06.
011
Wang, X., Gao, Y., Feng, Y., Li, X., Wei, Q., and Sheng, X. (2014). Cadmium stress
disrupts the endomembrane organelles and endocytosis during Picea wilsonii
pollen germination and tube growth. PLoS ONE 9:e94721. doi: 10.1371/journal.pone.0094721
Wang, Y., Huang, J., and Gao, Y. (2012). Arbuscular mycorrhizal colonization
alters subcellular distribution and chemical forms of cadmium in Medicago
sativa L. and resists cadmium toxicity. PLoS ONE 7:e48669. doi: 10.1371/journal.pone.0048669
Webster, E. A., and Gadd, G. M. (1996). Cadmium replaces calcium in the cell wall
of Ulva lactuca. Biometals 9, 241–244. doi: 10.1007/BF00817922
Weng, B., Xie, X., Weiss, D. J., Liu, J., Lu, H., and Yan, C. (2012). Kandelia
obovata (S., L.) Yong tolerance mechanisms to cadmium: subcellular distribution, chemical forms and thiol pools. Mar. Pollut. Bull. 64, 2453–2460. doi:
10.1016/j.marpolbul.2012.07.047
Wierzbicka, M. H., Przedpelska, E., Ruzik, R., Ouerdane, L., Polec-Pawlak, K.,
Jarosz, M., et al. (2007). Comparison of the toxicity and distribution of cadmium and lead in plant cells. Protoplasma 231, 99–111. doi: 10.1007/s00709006-0227-6
Wolf, S., Hematy, K., and Hofte, H. (2012). Growth control and cell wall signaling in
plants. Ann. Rev. Plant Biol. 63, 381–407. doi: 10.1146/annurev-arplant-042811105449
Wolff, G., Pereira, G. C., Castro, E. M., Louzada, J., and Coelho, F. F. (2012). The
use of Salvinia auriculata as a bioindicator in aquatic ecosystems: biomass and
structure dependent on the cadmium concentration. Braz. J. Biol. 72, 71–77. doi:
10.1590/S1519-69842012000100009
Wong, C. K. E., and Cobbett, C. S. (2009). HMA P-type ATPases are the major
mechanism for root-to-shoot Cd translocation in Arabidopsis thaliana. New
Phytol. 181, 71–78. doi: 10.1111/j.1469-8137.2008.02638.x
Wu, G., Kang, H., Zhang, X., Shao, H., Chu, L., and Ruan, C. (2010). A critical
review on the bio-removal of hazardous heavy metals from contaminated soils:
issues, progress, eco-environmental concerns and opportunities. J. Hazard.
Mater. 174, 1–8. doi: 10.1016/j.jhazmat.2009.09.113
Xin, J., Huang, B., Yang, J., Yang, Z., Yuan, J., and Mu, Y. (2013). Role of roots in
cadmium accumulation of two water spinach cultivars: reciprocal grafting and
histochemical experiments. Plant Soil 366, 425–432. doi: 10.1007/s11104-0121439-5
Xing, J. P., Jiang, R. F., Ueno, D., Ma, J. F., Schat, H., McGrath, S. P., et al. (2008).
Variation in root-to-shoot translocation of cadmium and zinc among different
March 2015 | Volume 6 | Article 133 | 15
Parrotta et al.
accessions of the hyperaccumulators Thlaspi caerulescens and Thlaspi praecox.
New Phytol. 178, 315–325. doi: 10.1111/j.1469-8137.2008.02376.x
Xiong, J., An, L., Lu, H., and Zhu, C. (2009). Exogenous nitric oxide enhances
cadmium tolerance of rice by increasing pectin and hemicellulose contents in
root cell wall. Planta 230, 755–765. doi: 10.1007/s00425-009-0984-5
Xiong, J., Fu, G., Tao, L., and Zhu, C. (2010). Roles of nitric oxide in alleviating heavy metal toxicity in plants. Arch. Biochem. Biophys. 497, 13–20. doi:
10.1016/j.abb.2010.02.014
Xu, J., Jia, R., Shi, G. X., Tian, X. L., Yang, H. Y., Xu, X. Y., et al. (2012a). Subcellular
distribution and phytotoxicity of cadmium in Alternanthera philoxeroides leaves.
Chi. J. Appl. Ecol. 23, 1070–1076.
Xu, J., Sun, J., Du, L., and Liu, X. (2012b). Comparative transcriptome analysis of
cadmium responses in Solanum nigrum and Solanum torvum. New Phytol. 196,
110–124. doi: 10.1111/j.1469-8137.2012.04235.x
Xu, W., Shi, W., Yan, F., Zhang, B., and Liang, J. (2011). Mechanisms of cadmium
detoxification in cattail (Typha angustifolia L.). Aquat. Bot. 94, 37–43. doi:
10.1016/j.aquabot.2010.11.002
Yamaguchi, N., Mori, S., Baba, K., Kaburagi-Yada, S., Arao, T., Kitajima, N., et al.
(2011). Cadmium distribution in the root tissues of solanaceous plants with
contrasting root-to-shoot Cd translocation efficiencies. Environ. Exp. Bot. 71,
198–206. doi: 10.1016/j.envexpbot.2010.12.002
Yang, J., and Pan, X. (2013). Root exudates from sunflower (Helianthus annuus L.)
show a strong adsorption ability toward Cd(II). J. Plant Interact. 8, 263–270. doi:
10.1080/17429145.2012.737030
Zhang, J., and Shu, W. S. (2006). Mechanisms of heavy metal cadmium tolerance
in plants. J. Plant Physiol. Mol. Biol. 32, 1–8.
Zhang, J., Wu, H., Wang, X., and Huang, W. (2010a). Subcellular distribution and
chemical forms of cadmium in the cells of strawberry (Fragaria × ananassa
Duch.). J. Hortic. Sci. Biotechnol. 85, 563–569.
Zhang, Z. C., Chen, B. X., and Qiu, B. S. (2010b). Phytochelatin synthesis plays
a similar role in shoots of the cadmium hyperaccumulator Sedum alfredii as
in non-resistant plants. Plant Cell Environ 33, 1248–1255. doi: 10.1111/j.13653040.2010.02144.x
Zhang, Q., Yan, C., Liu, J., Lu, H., Duan, H., Du, J., et al. (2014a). Silicon alleviation
of cadmium toxicity in mangrove (Avicennia marina) in relation to cadmium
compartmentation. J. Plant Growth Regul. 33, 233–242. doi: 10.1007/s00344013-9366-0
Frontiers in Plant Science | Plant Genetics and Genomics
The cell wall against cadmium
Zhang, S. J., Li, T. X., Huang, H. G., Zhang, X. Z., Yu, H. Y., Zheng, Z. C., et
al. (2014b). Phytoremediation of cadmium using plant species of Athyrium
wardii (Hook.). Int. J. Environ. Sci. Tech. 11, 757–764. doi: 10.1007/s13762-0130384-z
Zhang, W., Lin, K., Zhou, J., Zhang, W., Liu, L., and Zhang, Q. (2014c). Cadmium accumulation, sub-cellular distribution and chemical forms in rice
seedling in the presence of sulfur. Environ. Toxicol. Pharmacol. 37, 348–353. doi:
10.1016/j.etap.2013.12.006
Zhimin, Y., Shaojian, Z., and Aitang, H. U. (1999). Subcellular accumulation of
cadmium in corn and wheat plants at different levels of phosphorus. Pedosphere
9, 169–176.
Zhou, B., Yao, W., Wang, S., Wang, X., and Jiang, T. (2014). The metallothionein
gene, TaMT3, from Tamarix androssowii confers Cd2+ tolerance in tobacco. Int.
J. Mol. Sci. 15, 10398–10409. doi: 10.3390/ijms150610398
Zhu, X. F., Lei, G. J., Jiang, T., Liu, Y., Li, G. X., and Zheng, S. J. (2012).
Cell wall polysaccharides are involved in P-deficiency-induced Cd exclusion in
Arabidopsis thaliana. Planta 236, 989–997. doi: 10.1007/s00425-012-1652-8
Conflict of Interest Statement: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be
construed as a potential conflict of interest.
Received: 27 October 2014; accepted: 19 February 2015; published online: 13 March
2015.
Citation: Parrotta L, Guerriero G, Sergeant K, Cai G and Hausman J-F (2015) Target
or barrier? The cell wall of early- and later-diverging plants vs cadmium toxicity:
differences in the response mechanisms. Front. Plant Sci. 6:133. doi: 10.3389/fpls.2015.
00133
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